Palaeobiology

PALAEOBIOLOGY A SYNTHESIS

An ichthyosaur embryo (skull length 6.5 cm) discovered in 1985 by collectors Robert and Peter

Langham; from the Lower Lias (Lower Jurassic) of the Somerset coast, U.K. On display at City of Bristol Museum & Art Gallery, U.K. (Photograph courtesy of Dept. of Geology, University of Bristol).

PALAEOBIOLOGY A SYNTHESIS

EDITED BY

DEREK E. G. BRIGGS Department of Geology University of Bristol Queen's Road Bristol BS8 lRJ

AND

PETER R. CROWTHER Department of Geology Bristol City Museums and Art Gallery Queen's Road Bristol BS8 lRL

ON BEHALF OF THE PALAEONTOLOGICAL ASSOCIA nON

b

Blackwell Science

© 1990 by Blackwell Science Ltd Editorial Offices: Osney Mead, Oxford 0)(2 OEL 25 John Street, London WClN 2BL

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British Library Cataloguing in Publication Data Palaeobiology: A Synthesis 1. Palaeobiology

1. Briggs, D.E.G.

H. Crowther, P.R.

560 Set by Setrite Typesetters Ltd, Hong Kong Printed and bound in Great Britain at the University Press, Cambridge The Blackwell Science logo is a trade mark of Blackwell Science Ltd, registered at the United Kingdom Trade Marks Registry

ISBN 0-632-02525-5 (Hbk) ISBN 0-632-03311-8 (Pbk) Library of Congress Cataloging-in-Publication Data Palaeobiology: A Synthesis. Includes index. 1. Palaeobiology

1. Briggs, D.E.G. QE721.E53

1989

H. Crowther, P.R. 560'.3'21

ISBN 0-632-02525-5 (Hbk) ISBN 0-632-03311-8 (Pbk)

88-35060

Contents

1.12 Hominids, 88

List of Contributors, ix

R. L. SUSMAN

Foreword, xiii L. R. M. COCKS

1

2

Major Events in the History of Life

2.1

3

1.1

Origin of Life,

1.2

Precambrian Evolution of Prokaryotes and

2.2

9

2.3

Precambrian Metazoans,

17

2.4

Origin of Hard Parts - Early Skeletal Fossils,

24

2.5 2.6

30

Evolutionary Faunas,

I· I·

SEI'KOSKI.

2.7 37 2.8

If

Early Diversification of Major Marine Habitats w. I. AUSICH & D.

I.

2.9

BOTTlER

I.

119

BENTON

Hierarchy and Macroevolution,

124

Patterns of Diversification,

130

Coevolution,

136

139

Adaptation,

1'. W. SKELTON

2.10 Evolution of Large Size, 147

R. B. RICKARDS

M.

1.7.3 Reefs, 52

I.

BENTON

2.11 Rates of Evolution - Living Fossils, 152 D. C. FISHER

c. T. SCRUTTON

2.12 Mass Extinction: Processes 2.12.1 Earth-bound Causes, 160

Terrestrialization

1.8.1 Soils, 57 V. P. WRIGHT

A. HALLAM

2.12.2 Extra-terrestrial Causes, 164

1.8.2 Plants, 60

D. IABLONSKI

D. EDWARDS & N. D. BURGESS

2.12.3 Periodicity, 171

1.8.3 Invertebrates, 64

I. I

1'. A. SELDEN

1.8.4 Vertebrates, 68

SEPKOSKI,

Ir

2.13 Mass Extinction: Events 2.13.1 Vendian, 179

A. c. MILNER

Flight

M. A. S. McMENAMIN

2.13.2 End-Ordovician, 181

1.9.1 Arthropods, 72

P.

R. I. WOOTTON

I.

BRENCHLEY

2.13.3 Frasnian-Famennian, 184

1.9.2 Vertebrates, 75

G. R. McGHEE.

K. I'ADIAN

1.10 Angiosperms, 79

Ir

2.13.4 End-Permian, 187

M. E. COLLINSON

D. H. ERWIN

1.11 Grasslands and Grazers, 84 I.

Red Queen Hypothesis,

S. CONWAY MORRIS

1.7.2 Plankton, 49

1.9

111

1'. W. SIGNOR

1.7.1 Infauna and Epifauna, 41

1.8

106

N. ELDREDGE

s. CONWAY MORRIS

1.7

Heterochrony,

M.

Late Precambrian-Early Cambrian Metazoan Diversification,

1.6

Microevolution and the Fossil Record,

K. I. McNAMARA

B. RUNNEGAR & s. BENGTSON

1.5

100

Speciation,

P. R. SHELDON

M. A. FEDONKIN

1.4

95

B. CHARLESWORTH

A. H. KNOLL

1.3

Molecular Palaeontology, G. B. CURRY

c. R. WOESE & G. WACHTERSHAuSER

Protists,

The Evolutionary Process and the Fossil Record

2.13.5 End-Triassic, 194

R. THOMASSON & M. R. VOORHIES

M.

v

I

BENTON

2.13.6 Cretaceous-Tertiary (Marine), 198

3.11.6 Holzmaden, 282

F. SURLYK

R. WILD

2.13.7 Cretaceous-Tertiary (Terrestrial), 203

3.11.7 Solnhofen Lithographic Limestones, 285

L. B. HALSTEAD

G. VIOHL

2.13.8 Pleistocene, 207 E. L. LUNDELIUS,

3.11.8 Grube Messel, 289 j.

Jr

L. FRANZEN

3.11.9 Baltic Amber, 294 3

T. SCHLOTER

Taphonomy 3.1

3.12 Completeness of the Fossil Record, 298

Decay Processes,

213

c. R. c. PAUL

P. A. ALLISON

3.2

The Record of Organic Components and the Nature of Source Rocks,

217

P. FARRIMOND & G. EGLINTON

3.3

Destructive Taphonomic Processes and Skeletal Durability,

223

4

Palaeoecology 4.1 4.2

Transport - Hydrodynamics

4.3

3.4.1 Shells, 227 j.

4.4

R. L. ALLEN

R. A. SPICER

3.4.3 Bones, 232 Fossil Concentrations and Life and Death Assemblages,

4.5

235

4.6

Obrution Deposits,

239

4.7 4.8 4.9

244

Populations,

M. E. TUCKER

P. A. ALLISON

3.8.3 Pyrite, 253

Stromatolites,

336

Reefs and Carbonate Build-Ups, Encrusters,

341

346

3.8.4 Phosphate, 256 L. PREV6T &

Taphofacies,

A. c. SCOTT

4.11 Trace Fossils, 355 S. G. PEMBERTON, R. W. FREY & T. D. A. SAUNDERS

4.12 Evidence for Diet, 362 j.

P. A. ALLISON

j.

E. POLLARD

4.13 Predation 4.13.1 Marine, 368 C. E. BRETT

LUCAS

258

4.13.2 Terrestrial, 373 j.

c. E. BRETT & S. E. SPEYER

3.10 Anatomical Preservation of Fossil Plants, 263

A. MASSARE & c. E. BRETT

4.14 Parasitism, 376 s. CONWAY MORRIS

A. c. SCOTT

3.11 Taphonomy of Fossil-Lagerstatten 3.11.1 Overview, 266 A. SEILACHER

3.11.2 Burgess Shale, 270 s. CONWAY MORRIS

3.11.3 Upper Cambrian 'Orsten', 274 MOLLER

3.11.4 Hunsriick Slate, 277 j.

330

Coloniality,

4.10 Reconstructing Ancient Plant Communities, 351

3.8.2 Carbonate Nodules and Plattenkalks, 250

j.

326

P. D. TAYLOR

Diagenesis

K.

322

B. R. ROSEN

3.8.1 Skeletal Carbonates, 247

3.9

Hydrodynamics,

S. M. AWRAMIK

D. E. G. BRIGGS

3.8

318

B. R. ROSEN

c. E. BRETT

Flattening,

Biomechanics,

M. LaBARBERA

F. T. FORSICH

3.7

314

G. B. CURRY

A. K. BEHRENSMEYER

3.6

Composition and Growth of Skeleton,

P. A. SELDEN

3.4.2 Plant Material, 230

3.5

307

B. RUNNEGAR

c. E. BRETT

3.4

Morphology, L. LUGAR

BERGSTROM

3.11.5 Mazon Creek, 279 G. c. BAIRD

4.15 Palaeopathology, 381 L. B. HALSTEAD

4.16 Trophic Structure, 385 j.

A. CRAME

4.17 Evolution of Communities, 391 A.

j.

BOUCOT

4.18 Biofacies, 395 P.

j.

BRENCHLEY

4.19 Fossils as Environmental Indicators 4.19.1 Climate from Plants, 401 R. A. SPICER

vii

Contents 5.10 Global Boundary Stratotypes 5.10.1 Overview, 471

4.19.2 Temperature from Oxygen Isotope Ratios, 403

J. w. COWIE

T. F. ANDERSON

4.19.3 Salinity from Faunal Analysis and Geochemistry, 406 J

5.10.2 Precambrian-Cambrian, 475 J. W. COWIE

5.10.3 Ordovician-Silurian, 478

D. HUDSON

4.19.4 Oxygen Levels from Biofacies and Trace Fossils, 408

c. R. BARNES & S. H. WILLlAMS

5.10.4 Silurian-Devonian, 480 c. H. HOLLAND

D. J. BOTTJER & C. E. SAVRDA

5.11 Fossils and Tectonics, 482

4.19.5 Depth from Trace and Body Fossils, 411 G. E

5

R. A. FORTEY & L. R. M. COCKS

FARROW

Taxonomy, Phylogeny, and Biostratigraphy 5.1

6

Infrastructure of Palaeobiology 6.1

Computer Applications in

Rules of Nomenclature

Palaeontology,

5.1.1 International Codes of Zoological and Botanical Nomenclature, 417

J

6.2

Practical Techniques

6.2.1 Preparation of Macrofossils, 499

M. E. TOLLlTT

5.1.2 Disarticulated Animal Fossils, 419

P. J. WHYBROW & w. LlNDSAY

6.2.2 Extraction of Microfossils, 502

R. J. ALDRIDGE

5.1.3 Disarticulated Plant Fossils, 421

R. J. ALDRIDGE

6.2.3 Photography, 505

B. A. THOMAS

5.1.4 Trace Fossils, 423

D

Analysis of Taxonomy and Phylogeny

D. CLAUGHER & 1'. D. TAYLOR

6.2.5 Determination of Thermal Maturity, 511

5.2.1 Overview, 425

J. E

R. A. FORTEY

6.3

5.2.2 Cladistics, 430

6.3.1 Collection Care and Status Material, 515

P. L. FOREY

P. R. CROWTHER

6.3.2 Collection Management and Documentation Systems, 517

A. J. CHARIG

5.2.4 Stratophenetics, 437

P. R. CROWTHER

r. D. GINGERICH

5.2.5 Problematic Fossil Taxa, 442

6.3.3 Exhibit Strategies, 519

s. BENGTSON

R. S. MILES

5.3

Analysis of Taxonomic Diversity,

5.4

Vicariance Biogeography,

445

6.4

Societies, Organizations, Journals, and Collections,

A. B. SMITH

448 6.5

Palaeobiogeography,

History of Palaeontology

6.5.1 Before Darwin, 537

452

c. R. NEWTON

J. c. THACKRAY

6.5.2 Darwin to Plate Tectonics, 543

Biostratigraphic Units and the Stratotypei Golden Spike Concept,

461

P. J

Zone Fossils, M. G

5.8

466

J. W. VALENTINE

6.5.4 The Past Decade and the Future, 550

BASSETT

International Commission on Stratigraphy,

468

A. HOFFMAN

M. G. BASSETT

5.9

International Geological Correlation Programme, J. W. COWIE

BOWLER

6.5.3 Plate Tectonics to Paieobioiogy, 547

c. H. HOLLAND

5.7

522

J. NUDDS & D. PALMER

L. GRANDE

5.6

A. MARSHALL

Museology

5.2.3 Evolutionary Systematics, 434

5.5

J. SIVETER

6.2.4 Electron Microscopy, 508

S. R. A. KELLY

5.2

493

A. KITCHELL

469

Index,

557

List of Contributors

R. J. ALDRIDGE

A. J. B 0 UCOT

Department of Geology, University

J. R. L. ALLEN ,

P.

Postgraduate Research Institute for

P.

A. ALLISON

J. BRENCHLEY

C. E. BRETT Department of Geology, Univer­

D. E. G. B RIGGS Department of Geology,

University

of Bristol, Queen's Road, Bristol BS8 1RJ, U.K.

Department of Geological Sciences,

Ohio State University, Columbus, Ohio 43210, U.5.A.

S. M. A WRAMIK

Department of Geological Sciences, Uni­

versity of Rochester, Rochester, New York 14627, U.S.A.

sity of Illinois, Urbana, Illinois 61801, U.5.A.

W. I. A USICH

Department of Earth Sciences,

U.K.

U.K.

T. F. ANDERSON

Department of Social Anthropology,

University of Liverpool, PO Box 147, Liverpool L69 3BX,

Postgraduate Research Institute for

Sedimentology, University of Reading, Reading RG6 2AB,

N. D. BURGESS

Royal Society for the Protection of

Birds, Sandy, Bedfordshire SG19 2DL, U.K.

Department of Geological Sciences,

University of California, Santa Barbara, California 93106,

A. J. CH A RIG

U.S.A.

G. C. BAIRD

J. BOWLER

Queen's University, Belfast BT7 1NN, U.K.

Sedimentology, University of Reading, Reading RG6 2AB, U.K.

P.

Department of Zoology, Oregon State

University, Corvallis, Oregon 97331, U.5.A.

of Leicester, Leicester LE1 7RH, U.K.

clo Department of Palaeontology, The

Natural History Museum, Cromwell Road, London SW7 5BD, U.K.

Department of Geosciences, State Univer­

sity of New York College: Fredonia, Fredonia, New York

B. CHARLESWORTH

14063, U.5.A.

C. R. BARNES

Chicago, Illinois 60637, U.S.A.

School of Earth and Ocean Sciences,

University of Victoria, P.O. Box 3055, Victoria, British

D. CL A UGHER

Columbia V8W 3P6, Canada.

M. G. BASSETT

Department

L.

Institute of Palaeontology, University

Egham Hill, Egham, Surrey TW20 OEX, U.K.

S. CONWA Y MORRIS

Department of Geology, University of

Sciences,

J. BERGSTROM Swedish Museum of Natural

Department of Geology, Royal

Holloway & Bedford New College, University of London,

Bristol, Queen's Road, Bristol BS8 1RJ, U.K.

University

Department

of Cambridge,

of

Earth

Downing Street,

Cambridge CB2 3EQ, U.K.

History,

J. W. COWIE

S-104 05

Department of Geology, University of

Bristol, Queen's Road, Bristol BS8 1RJ, U.K.

Stockholm, Sweden.

D. J. BOTTJER

Department of Palaeontology, The

M. E. COLLINSON

of Uppsala, Box 558, S-751 22 Uppsala, Sweden.

PO Box 50007,

R. M. COCKS 5BD, U.K.

Institution, Washington DC 20560, U.5.A.

Section of Palaeozoology,

The

Natural History Museum, Cromwell Road, London SW7

of Paleo­

biology, National Museum of Natural History, Smithsonian

M. J. BENTON

of Mineralogy,

5BD, U.K.

Department of Geology, National

A. K. BEHRENSMEYER

Department

Natural History Museum, Cromwell Road, London SW7

Museum of Wales, Cathays Park, Cardiff CFl 3NP, U.K.

S. BENGTSON

Department of Ecology and

Evolution, University of Chicago, 1103 East 57th Street,

J. A. CRAME

Department of Geological Sciences,

British Antarctic Survey, High Cross,

Madingley Road, Cambridge CB3 OET, U.K.

University of Southern California, Los Angeles, California 90089, U.5.A.

P.

R. CROWTHER

Bristol City Museums & Art

Gallery, Queen's Road, Bristol BS8 1RL, U.K. ix

List of Contributors

x

G. B. CURRY Department of Geology

Applied

&

Geology, University of Glasgow, Glasgow G12 8QQ, U.K.

D. EDWARDS Department of Geology, University of Wales College of Cardiff Cathays Park, Cardiff CFl 3YE, U.K.

G. EGLINTON Organic Geochemistry Unit, School of Chemistry, University of Bristol, Bristol BS8 l TS, U.K.

N. ELDREDGE

Department

of

Invertebrates,

American Museum of Natural History, Central Park West at 79th Street, New York, NY 10024, U.S.A.

D. H. ERWIN Department of Palaeobiology, National Museum of Natural History, Smithsonian Institution, Washington DC 20560, U.S.A.

P. FARRIMOND The Organic Geochemistry Unit, The University, Newcastle upon Tyne NEl 7R U, U.K.

G. E. FARROW 19 Glenburn Road, Bearsden, Glasgow G61 4PT, U.K.

M. A. FEDONKIN

Palaeontological

Institute,

U.S.S.R. Academy of Sciences, Moscow 117321, U.S.S.R.

D. C. FISHER Museum of Paleontology, University of Michigan, Ann Arbor, Michigan 48109, U.5.A.

P. L. FOREY

Department

of

Palaeontology,

The

5BD, U.K. The

Natural History Museum, Cromwell Road, London SW7 5BD, U.K.

J. L. F RANZEN

Forschungsinstitut

Senckenberg,

Senckenberganlage 25, D-6000 Frankfurt am Main 1, Germany.

R. W. FREY

Institut

for

Paliiontologie

der

Universitiit, Pleicherwall 1, D-8700 Wiirzburg, Germany.

P. D. GINGERICH

C. H. HOLLAND Department of Geology, Trinity ' College, Dublin, Ireland.

J. D. HUDSON Department of Geology, University of Leicester, University Road, Leicester LEl 7RH, U.K. Department

D. JAB L 0 NSKI

of

the

Geophysical

Sciences, University of Chicago, 5734 S. Ellis Avenue, Chicago, Illinois 60637, U.5.A.

S. R. A. K ELLY British Antarctic Survey, High Cross, Madingley Road, Cambridge CB3 OET, U.K.

J. A. KITCHELL Museum of Paleontology, Univer­ sity of Michigan, Ann Arbor, Michigan 48109, U.5.A.

A. H. KN 0 LL Department of Organismic lutionary

Biology,

Harvard

University,

& Evo­

Cambridge,

Massachusetts 02138, U.S.A.

M. LaBARBERA Department of Anatomy, Univer­ sity of Chicago, 1025 East 57th Street, Chicago, Illinois 60637, U.S.A.

'vV. LINDSAY

Department

of

Palaeontology,

The

Natural History Museum, Cromwell Road, London SW7

J. LUCAS Institut de Geologie, Universite Louis Pasteur, 1 rue Blessig, Strasbourg 67084, France.

L. LUGAR Department of Geology, Franklin

& Marshall

College, Lancaster, Pennsylvania 17604, U.5.A.

E. L. LUNDELIUS, Jr Department of Geological Sciences, University of Texas, Austin, Texas 78713, U.S.A.

J. E. A. MARSHALL Department of Geology, The University, Highfield, Southampton S09 5NH, U.K.

J. A. MASSARE Department of Geological Sciences,

Deceased.

F. T. FURSICH

Deceased.

5BD, U.K.

Natural History Museum, Cromwell Road, London SW7

R. A. FORTEY Department of Palaeontology,

A. HOFFMAN

Museum

of

Paleontology,

University of Michigan, Ann Arbor, Michigan 48109, U.5.A.

L. GRANDE Department of Geology, Field Museum of Natural History, Chicago, Illinois 60605, U.S.A.

A. HALLAM School of Earth Sciences, University of Birmingham, PO Box 363, Birmingham B15 2TT, U.K.

L. B. HALSTEAD Deceased.

University of Rochester, Rochester, New York 14627, U.5.A.

G. R. MeGHEE, Jr Sciences,

Rutgers

Department

University,

New

of

Geological

Brunswick,

New

Jersey 08903, U.S.A.

M. A. S. MeMENAMIN Department of Geology Geography,

Mount

Ho/yoke

College,

South

&

Hadley,

Massachusetts 01075, U.5.A.

K. J. MeNAMARA Western Australian Museum, Francis Street, Perth, Western Australia 6000, Australia.

List of Contributors R.

S.

MILES Department

of

Public

Services,

The

Natural History Museum, Cromwell Road, London SW7 5BD, U.K.

A.

C.

MILNER Department

of

Palaeontology,

The

C.

A.

P.

A.

University

Chicago, Illinois 60637, U.S.A. P.

R.

of Wales, Cathays Park, Cardiff CFl 3NP, U.K. Department

of

Earth

Sciences,

U.K. G.

P.

PEMBERTON Department of Geology, Uni­

J. E. POLLARD Department of Geology, University of Manchester, Oxford Road, Manchester M13 9PL, U.K.

Strasbourg 67084, France. B.

P.

of

Earth

of

Palaeontology,

The

Natural History Museum, Cromwell Road, London SW7

A.

RUNNEGAR Institute of Geophysics & Planetary

California 90024, U.5.A. SAUNDERSDepartment of Geology, Uni­

SAVRDA Department

of

Geology,

Auburn

University, Auburn, Alabama 36849, U.S.A.

T. SCHLUTER Department of Geology, C.

B.

SMITH Department

of

Palaeontology,

The

E.

SPEYER Department of Geology, Arizona State

R.

A.

SPICERDepartment of Earth Sciences, Univer­

F. SURLYK Geological Institute, University of Copen­ hagen,

0ster

Voldgade 10,

DK-1350 Copenhagen K,

R.

Makerere

SCOTT Department of Geology, Royal Holloway

& Bedford New College,

University of London, Egham

Hill, Egham, Surrey TW20 OEX, U.K.

L.

SUSMAN Department of Anatomical Sciences,

State University of New York, Stony Brook, Long Island, New York 11794, U.S.A. P.

D.

TAYL0 R Department

of

Palaeontology,

The

Natural History Museum, Cromwell Road, London SW7 5BD, U.K.

J. C. THACKRAY Archivist, The Natural History Museum, Cromwell Road, London SW7 5BD, U.K.

University, PO Box 7062, Kampala, Uganda. A.

W. SKELTON Department of Earth Sciences,

University, Tempe, Arizona 85287-1404, U.S.A.

versity of Alberta, Edmonton, Alberta T6G 2E3, Canada. E.

University

5BD, U.K.

versity of California, 405 Hilgard Avenue, Los Angeles,

C.

Collections,

Denmark.

Physics and Department of Earth & Space Sciences, Uni­

A.

Geology

Natural History Museum, Cromwell Road, London SW7

5BD, U.K.

D.

J. SIVETER

sity of Oxford, Parks Road, Oxford OXl 3PR, U.K.

B. R. R0 SEN Department

T.

SIGNORDepartment of Geology, University of

U.K.

Sciences, Cambridge

CB2 3EQ, U.K.

B.

Sciences,

Open University, Walton Hall, Milton Keynes MK7 6AA,

S.

RICKARDS Department

Earth

Museum, Parks Road, Oxford OXl 3PW, U.K.

L. PREV6T Centre de Geochimie, CNRS, 1 rue Blessig,

University of Cambridge, Downing Street,

W.

D.

versity of Alberta, Edmonton, Alberta T6G 2E3, Canada.

R.

of

California, Davis, California 95616, U.S.A.

University of Liverpool, PO Box 147, Liverpool L69 3BX, S.

SHELDON Department

Open University, Walton Hall, Milton Keynes MK7 6AA, U.K.

D. PALMER Department of Geology, National Museum PAUL

SELDEN Department of Geology, University of

Sciences, University of Chicago, 5734 S. Ellis Avenue,

of California, Berkeley, California 94720, U.S.A.

C.

Connecticut

J. J. SEPK0 SKI, Jr Department of the Geophysical

PADIAN Department of Paleontology,

R.

Yale University, New Haven,

Manchester, Oxford Road, Manchester M13 9PL, U.K.

NEWTON Department of Geology, Syracuse

chester, Oxford Road, Manchester M13 9PL, U.K.

C.

Geological

06511, U.S.A.

J. NUDDS Manchester Museum, University of Man­

K.

of

10, D-7400 TUbingen 1, Germany, and Kline Geology

J. MULLER Rheinische F.-W. Universitiit, Institut

University, Syracuse, New York 13244, U.S.A.

Department

SEILACHER Institut und Museum fUr Geologie

Laboratory,

fUr Paliiontologie, Nusallee 8, D-5300 Bonn 1, Germany. R.

SCRUTTON

und Paliiontologie, Universitiit TUbingen, Sigwartstrasse

Natural History Museum, Cromwell Road, London SW7

C.

T.

Sciences, University of Durham, Durham DHl 3LE, U.K.

5BD, U.K. K.

xi

B.

A.

THOMAS Department

of

Botany,

National

Museum of Wales, Cathays Park, Cardiff CFl 3NP, U.K.

J. R. THOMASSON Department of Biology and Allied Health, Fort Hays State University, Hays, Kansas 67601, U.S.A.

List of Contributors

xii M.

E.

TOLLITT Department of Public Services, The

R.

5BD, U.K. M.

E.

S.

TUCKER Department of Geological Sciences,

Sciences,

University

of

VIOHL Jura

Department

of

Geological

California,

Santa

Barbara,

C.

R.

Museum,

University

Willibaldsburg,

0-8078

of

Nebraska,

W.A.CHTERSH.A.USER

of

Nebraska

R.

WILLIAMS Department

of

Earth

Sciences,

R.

WOESE Department of Microbiology, University

J. WOOTTON Department of Biological Sciences,

Lincoln,

4PS, U.K.

State

Nebraska

V.

P. WRIGHT Postgraduate Research Institute for Sedimentology, University of Reading, Reading RG6 2AB,

Tal

29,

0-8000

MUnchen 2, Germany.

P. J. WHYBROW Department of Palaeontology, The Natural History Museum, Cromwell Road, London SW7 5BD, U.K.

H.

University of Exeter, Prince of Wales Road, Exeter EX4

68588, U.S.A. G.

Naturkunde,

Urbana, Illinois 61801, U.5.A.

VOORHIES University

Museum,

fUr

of Illinois, 131 Burrill Hall, 407 South Goodwin Avenue,

Eichstatt, Germany. M.

Museum

Canada.

California 93106, U.S.A. G.

Staatliches

Memorial University, St John's, Newfoundland AIB 3X5,

University of Durham, Durham DHl 3LE, U.K.

J. W. VALENTINE

WILD

Rosenstein 1, 0-7000 Stuttgart 1, Germany.

Natural History Museum, Cromwell Road, London SW7

U.K.

Foreword L. R . M . C O C K S President of the Palaeontological Association 1986-1988

dition to its twin periodicals Palaeontology and Special Papers in Palaeontology, and we are particu­ larly pleased at the international response to our call for contributions, all of which have been received within a very tight timetable . However, the Association's most particular and special thanks must go to Derek Briggs and Peter Crowther, who, from the twin venues of the Univer­ sity and City Museum at Bristol, have cheerfully and enthusiastically master-minded the whole pro­ ject from its inception . Their contributions of time and effort, willingly given at the Association' s re­ quest, have culminated so effectively in the present volume . Blackwell Scientific Publications have also proved excellent partners, and have brought all their renowned publishing expertise into the pro­ duction of this book . I cannot close without reiterating what a chal­ lenging and exciting time this is for palaeontology . During the nineteenth century the dating of rocks by fossils was at the very leading edge of geological studies, but for the middle years of this century it was displaced from that central position as the new generation of machine-led scientists made quali­ tative comparisons of fossils seem old-fashioned and peripheral . However, this very volume demon­ strates how that latter position has changed, and that palaeontological and palaeobiological studies are now at the heart of a host of scientific themes ranging from evolutionary biology, through the dis­ position of continental plates in ancient oceans, to direct use in the search for oil . These changes have been accompanied by much quantitative reassess­ ment of biotas and much new machinery . Individual palaeontologists have responded vigorously to these challenges and our horizons are already expanding in all dimensions into the next century .

Scientists, both professional and amateur, have been describing fossils for over 200 years and the fruits of their labours make long library shelves groan with monographs and periodicals . These fruits have been distilled many times into the varied palaeontological textbooks and other encyclopaedic essays, which, in the case of the most common fossils, the inver­ tebrate animals, have culminated in the many vol­ umes of the Treatise on Invertebrate Paleontology. It is not our aim to compete with them . This is not an encyclopaedia of palaeontology . Why then another book? In fact the very virtues and comprehensiveness of the Treatise and other compilations have enabled many scientists to add extra dimensions to their studies over the past 20 years, and it is the fruits of this vintage crop which are assembled here . Palaeobiology has come to en­ compass the heady topics of evolution, ecology and the subsequent taphonomy of extinct animals and plants, and articles on these are gathered here in over 120 contributions by leading workers from a variety of countries . General descriptions of the morphology of fossils are omitted, but the book includes background sections on general taxonomy, biostratigraphy and techniques, and a tantalizing group of essays in which the historical background to our science is placed in perspective . Each of the contributions reflects the individuality of its authors, but we trust that each article is complete in itself (and many will no doubt directly refresh a continuing lecture course) . For over 30 years the Palaeontological Association has been the focal point in Britain for studies on fossils . This book is not merely sponsored by the Association, but was generated in outline round its Council table . It forms one of a line of continuing substantial publications by the Association in ad-

xiii

1 MAJOR EVENTS IN THE HISTORY OF LIFE

The Jurassic pterosaur Pterodactylus kochi from Solnhofen Limestone preserving impressions of the wing membranes, x 0.84. (Photograph courtesy of J.M.V. Rayner.)

1.1 Origin of Life C. R . WOESE & G . WACHTERSHAuSER

Introduction

allusion has had a significant impact on later think­ ing, undoubtedly far more than its author intended or would have liked. Oparin (1924 in Bernal 1967) and Haldane (1929 in Bernal 1967) are generally credited with formulating the issue scientifically; not because they were the first to attempt it, but because their origin scenarios were more compre­ hensive than those of their predecessors. The details of these theories need not concern us; for they often reflected misconceptions, for example as to the nature of genes, viruses, and protoplasm, and how they replicate. However, in their general aspects the theories are of great interest, for, remarkably, these half century old proposals still remain the foundation of our understanding of life's beginnings. The Oparin ocean scenario has by now become almost catechismaL It begins with a primitive anoxic atmosphere, comprising gases such as carbon diox­ ide or methane, nitrogen or ammonia, hydrogen sulphide, water, and hydrogen. Current thinking invokes the less reduced forms of these elements, the fully reduced forms being postulated earlier, by Urey (1951 ) and others, on the mistaken as­ sumption that the nascent Earth possessed an at­ mosphere similar to those found on the large gaseous planets. Miller (1953 ) was the first to put such models to scientific tests when, as a student in the nineteen-fifties, he demonstrated that electrical discharge acting on Urey's atmosphere produced a conglomeration of organic compounds that included many of the familiar amino acids. The many experi­ ments that followed showed that not only amino acids, but also a variety of organic compounds of biological interest, can be produced by a variety of energy sources under a variety of conditions (pro­ viding that oxygen is absent). So today we believe that some anoxic, slightly reducing atmosphere, acted upon by ultraviolet light and/or electrical dis­ charge, served as a continual source of the simple reactive organic chemicals needed to begin and sustain the evolutionary process. The products of this atmospheric chemistry ended up in the primitive ocean, which over time became a vast repository of reactive organic chemicals. Oparin's and Haldane's primitive ocean was a 'hot

The origins of man and his fellow creatures are concerns perhaps as old as man himself. However, before the nineteenth century these could not be given scientific form. The prescientific notions of life's beginnings were an incongruous amalgam of biblical thought, philosophy, alchemy and folk wisdom. The Bible taught that all life arose through special acts of divine creation during the first days of the Earth's existence. Commonplace experience showed, however, that life can also arise spon­ taneously, as maggots seemed to, for example, from rotting meat. And vitalism saw life as an ever­ present non-material property of the universe. In the nineteenth century four great scientific achievements laid the groundwork for making the origin of life a scientific problem: (1 ) The realization that the cell was the fundamental unit of biology introduced an enormous gulf between the living and non-living worlds; (2 ) Darwin's theory of evo­ lution implied that all life came from some distant universal ancestor; (3 ) Pasteur painstakingly and convincingly refuted the claims of spontaneous generation (of microscopic life); so that, if life had arisen spontaneously on this planet, it must have done so under conditions no longer present and probably long gone; and (4 ) Mendel discovered genetics, whose origin is to this day one of biology's great mysteries. The picture we now have of life's origin, though scientific, is based upon very few facts. It derives mainly from metaphysical assumptions, cultural images we take for granted. Consequently, it is likely to share features with the prescientific ac­ counts of life's origin which go unrecognized and unchallenged. The present discussion of origins is framed along historical lines, a format that generally helps to reveal prejudices that impede or sidetrack the development of a scientific picture. The conventional primitive ocean scenario

Darwin apparently gave little thought to the origin of life; he understood the problem to be intractable in his time. However, his casual 'warm little pond' 3

4

1

Major Events in the History of Life

dilute soup' (Haldane's phrase); hot on the mistaken assumption (common in the nineteen-twenties) that the Earth had arisen as a fragment of the Sun. With the later acceptance of a cold accretion model for the Earth's formation (also incorrect), the oceanic soup was cool from the start. The primitive ocean, then, was a 'vast chemical laboratory', a cosmic retort in which the great alchemist Nature sought to concoct the first living cell. The most important but weakest element in the ocean scenario is the transition from prebiotic chemistry to actual living, self-replicating entities. The early models necessarily resorted to hand waving arguments - interactions occurring among the reactive chemicals in the primitive ocean led to ever more complex structures, to more and more complicated aggregates, that ultimately somehow became self-perpetuating. Later proposals, drawing upon the structure of nucleic acid, refined this no­ tion to that of macromolecular templating. As Haldane (1929 ) put it, in the ocean 'the first precursors of life found food available in consider­ able quantities'. Therefore, there was no need for them to evolve the capacity to produce these metab­ olites, and so they did not. The aboriginal organisms were total heterotrophs. This seldom questioned assertion determines the subsequent evolutionalY course. A heterotrophic life style will necessarily (and rather quickly in evolutionary terms) deplete the oceanic stores of nutrients. If organisms are then to survive, they must evolve an intermediary metabolism and eventually learn to transduce other forms of energy (light or chemical) into biochemical energy. The current explanation for how intermediary metabolism arose in the aboriginal heterotrophs was fashioned by Horowitz (1945 ). When the oceanic supply of a particular amino acid, for example, became exhausted, the supply of its im­ mediate chemical precursor, for example an hydroxy acid (for which organisms previously had had no need), still remained untapped. Were the organism to evolve an enzy me that converted this precursor to the needed amino acid at this point both the organism and its progeny would survive. When, sometime later, the supply of the precursor also became exhausted, the process would repeat - the organism evolving another enzyme to catalyse syn­ thesis of the precursor from its own (previously unutilized) precursor; and so on. In this manner all intermediary metabolism arose, the pathway s evolving 'backward', one step at a time. Neither Oparin nor Haldane initially postulated

cellular entities as a starting point for evolution, although Oparin did so later, with his coacervate model. There has been no subsequent consensus as to when cellularity arose. Criticisms of and refinements to the standard model

The essence of the primitive ocean scenario (i. e. its metaphysics) has never been seriously questioned. However, many weaknesses in its details have come to light over the years. In each case the tendency has been to correct the problem by adding some new feature to the model. As a result today's origin scenario is a Ptolemaic hodgepodge of ad hoc as­ sumptions. There is little point any longer in criti­ cizing the standard model simply in the standard way, adding another ad hoc feature to remedy each new difficulty. The basic (implicit) assumptions of the model must be questioned. Cultural roots of the primitive scenario. Although the Oparin ocean scenario was developed as a scientific alternative to the prescientific versions of the pro­ cess, its similarity to the Garden of Eden myth should be worrisome. An oceanic 'paradise' is pos­ tulated in which organisms can develop safely in the midst of plenty. In addition to having 'food available in considerable quantities', the first or­ ganisms 'had no competitors in the struggle for existence' (Haldane 1929 ). Scientists have tended to see the first organism as arising through a series of highly unlikely events; discussions centre about improbable happenings that, given long times and enormous numbers of trials, eventually come to pass. (Remember that before the discovery of micro­ fossils the Earth was generally thought to have been sterile for most of its existence, allowing billions of years for key events to happen. ) Yet none of this is regarded as miraculous! One can even detect something akin to the biblical banishment in the scientific account: because or­ ganisms ultimately destroyed their oceanic paradise (by consuming the store of biochemicals), they were thrust into a harsh world where they had to fend for themselves by developing intermediary metabo­ lism, autotrophy, and eventually phototrophy. This was the dog-eat-dog world of competitive existence: 'The further life progressed the less nutrient sub­ stances were available to the organisms and the more strongly and bitterly the struggle for existence was waged' (Oparin 1 924 ). Its truth aside, the Oparin ocean scenario seems a prime example of culturally

1.1

Origin of Life

determined imagery shaping a scientific concept. The sooner these cultural influences are recognized and understood, the sooner a proper scientific pic­ ture of the origin of life will emerge. With a need for major restructuring in mind, let us analyse the main elements in the standard scen­ ario in detail. Energy sources, the multi-theatre assumption, and the ocean repository. The ultraviolet light or electrical discharge invoked by the standard scenario to create the initial simple reactive compounds are so ener­ getic that they produce indiscriminate bond rup­ tures, ionizations and free radicals. These would be entirely destructive of any larger (organic) compounds, not to mention living systems. This dilemma forces the standard scenario into a 'two­ theatre' assumption: the initial simple reactive com­ pounds produced in one theatre (the atmosphere) are subsequently quenched and protected in a se­ cond theatre (the ocean), where they accumulate and further react to produce more complex struc­ tures, and ultimately living systems. The need for two widely separated theatres seems to underlie a pernicious paradox in the standard scenario: the notion of reactive chemicals is at odds with their transport over great distances, from the high atmosphere to the ocean. The ocean must accumulate reactive chemicals over long times be­ cause distance necessarily translates into dilution. A protracted accumulation (and storage) in turn is at odds with the reactivity of these chemicals and their rapid removal by hydrolysis or sedimentation. In retrospect it is strange that all attempts to correct the difficulties with this oceanic chemical repository-reaction pot have never questioned its underlying multi-theatre assumption. Rather, dif­ ficulties were overcome by invoking additional theatres. Mineral surfaces, particularly clays, were seen by Bernal (1 967) as a vehicle for concentrating and reacting organic chemicals. He pictured the dilute organic compounds in the ocean becoming concentrated in the froth that forms on its surface, the froth being driven shoreward, to end up in estuaries - where the already concentrated com­ pounds became even more so in the oozes that formed there. Organic compounds adsorbed in high concentrations on clay sediments (and perhaps oriented and/or activated in the process) might then undergo spontaneous condensations, to pro­ duce biopolymers, and so on. Considerable experi­ mental work has been done, e. g. by Katchalsky (1973 ) and co-workers, on the properties of clay

5

minerals vis-a-vis the adsorption and reactivity of organic compounds. We shall encounter below a fundamentally different role for surfaces in the ori­ gin of life. Fox (1965 ) demonstrated experimentally that mix­ tures of amino acids (rich in the dicarboxylic amino acids) polymerized under hot (less than 200 0 C) non-aqueous conditions. Upon hydration these condensates produced 'proteinoid microspheres', which loosely resembled cells (in size, shape, and in having a few general catalytic properties). Because of this Fox argued that the high temperature con­ ditions associated with volcanic environments were those under which the organic compounds in the ocean repository bp came concentrated and re­ acted to give the prototypes of living systems. Invoking additional theatres is a Ptolemaic solu­ tion to the standard scenario's problems - which to a large extent are due to the multi-theatre as­ sumption. The true remedy may lie in single-theatre scenarios, in which the energy source can be in close proximity to or within the evolving system. These are conditions under which an energy flux can constantly generate a rich spectrum of organic biochemicals that are turned over rather than stored. The organism-environment dichotomy; heterotrophy and self-assembly. For a sufficiently primitive system, the organism-environment distinction does not exist. The dichotomy arises only when the evolving system has become sufficiently complex and physi­ cally separated from its surroundings that it can be viewed as an entity in its own right. However, the standard scenario (shaped by the properties of extant life) tends to see an organism-environment dichotomy early in the evolutionary process certainly too early. What occurs in the 'organism' is strongly distinguished from what occurs in its 'en­ vironment'. The dichotomy (together with the Garden of Eden image) then makes of the ocean repository a pre-existing store of 'food' for the abor­ iginal organisms. They, in turn, come into being as heterotrophs, and go on to deplete and ultimately exhaust their store of food. In other words, a prema­ turely forced distinction between organism and en­ vironment tends to place the replicative aspect of the primitive system in the former, its metabolic aspect in the latter. In such a dichotomous world the environment does not naturally, automatically, give rise to the organism. The latter has to 'strive' to bring itself into existence; it is the product of accidental self-assembly from simpler components in the

6

1

Major Events in the History of Life

environment - an improbable and, therefore, pro­ tracted process. (Subject to the vagaries of chance in this way the evolutionary process has to pass through a stage of instability, of uncertain outcome. ) A more extensive quote from Haldane shows these features rather clearly: 'When the whole sea was a vast chemical laboratory the conditions for the formation of such films [membranes, that is] must have been relatively favourable; but for all that life may have remained in the virus ... half­ living chemical ... stage for many millions of years before a suitable assemblage of elementary units was brought together in the first cell. There must have been many failures, but the first successful cell had plenty of food. ' Were life to have originated in an autotrophic rather than heterotrophic manner, the scenario would have been markedly different. Autotrophic evolution focuses on autocatalytic reaction net­ works, on metabolic pathways - whence all other evolutionary developments stem. It is a single theatre scenario, in which energy source, production of reactive compounds, and condensations to form complex organic structures, occupy the same locale. When life begins with autotrophic metabolic path­ ways, one avoids the kind of dichotomous sepa­ ration that exists between a heterotrophic organism and its host environment. An autotrophic system is a source of biochemical energy and complexity, not a sink for these (as are heterotrophs). With auto­ trophy the protracted, chancy trial and error period no longer seems required; the self-replicating entity (its genetics) can arise simply as a more refined and complex extension of the primary autotrophic and autocatalytic process. While some self-assembly might have to occur even in this process, that requirement too can be reduced by eliminating the constancy of the chemical conditions. In other words, major changes in the evolving system could be driven by, or be responses to, local or global changes in the state of the planet. The origin of genetics; templating and the genotype! phenotype dichotomy. Mendel's great discovery, that the cell has a phenotypic-functional aspect that is determined by a cryptic genotypic-reproductive aspect, has dominated our view of the origin of life. With the discovery in the nineteen-forties that each gene corresponds to a unique enzyme, the central question could then be phrased: 'Which came first, the gene or the enzyme?' Geneticists such as H. J. Muller felt that the gene had to have come first; only a few physiologists disagreed. (The gene at that

time was often thought of as proteinaceous and even as having its own primitive phenotype. ) Watson and Crick's discovery of the double stranded structure of nucleic acid rendered the question meaningless. Since all genes appeared to have the same basic structure, they could not have unique phenotypes, could not be functional in their own right; and, proteins (i. e. enzymes) could not evolve without genes - a chicken and egg paradox. At this point the central question should have become 'How did the genotype-phenotype re­ lationship (i. e. translation) arise?' However, the attractive and specific mechanism for the origin of gene replication inherent in the double stranded structure for nucleic acid (plus our near total ignor­ ance of the molecular mechanics of translation) took us in an opposite direction. The origin of the geno­ type (nucleic acid replication) separated completely from the origin of the phenotype (metabolism) the former question totally eclipsing the latter (Eigen et al. 1981 ; Orgel 1973 ). Recently it has be­ come popular to believe that (RNA based) 'nucleic acid life' must have preceded protein-based life; that initially nucleic acid was both the genotype and the phenotype. This point of view is supported by the facts: (1 ) that polypyrimidines can serve as templates that align complementary purine nucleo­ tides, which (when properly activated) then go on to condense into polypurine chains; and (2 ) that some RNAs possess certain limited enzymatic or catalytic properties. Eigen has also reported that in the presence of a particular protein (the replicase of the virus Q�) a certain type of RNA will spontaneously arise (in the absence of a pre-existing template). A fascinating variation on the templating theme is Cairns-Smith's (1985 ) proposal that life began with replicating patterns in clay layers (which could adsorb organic molecules and thereby influence the course of subsequent organic evolution). While daring in one way, this proposal is conventional in another; it takes for granted the need for templating as an initial step in the origin of life. A totally dichotomous view of the origins of the genotype (replication) and the phenotype (metab­ olism) is an extrapolation in the wrong direction. It has even led Dyson (1985 ) to propose that life arose twice; initially somehow as protein-based life, within which nucleic acid then separately arose as a 'disease'. The earliest life forms were almost cer­ tainly not incarnations of our dichotomies, of our attempts to define extant life. Rather, primitive living systems were undoubtedly less well de-

1.1

7

Origin of Life

fined, less compartmentalized, than their modern counterparts, and so in that unusual sense more 'integrated'. It is time to reassess the genotype­ phenotype dichotomy as a paradigm for the origin of life. A proper conceptualization of translation, the process that defines the genotype-phenotype re­ lationship, should have an integrating, unifying effect on our concept of the origin of life. Unfortu­ nately, the translation mechanism is large and com­ plex, and, therefore, its molecular workings and evolution are not understood. The fact that some of the proteins involved in translation are also com­ ponents of certain nucleic acid replication enzymes, however, suggests primitive connections between the two processes. The facts that cells today contain transfer RNA-like molecules as essential parts of non-translational ('non-programmed') polymeriz­ ations (e. g. polypeptide antibiotic and cell wall syn­ theses), and that nucleotides, other heterocyclic compounds, and even transfer RNAs play important roles in intermediary metabolism, hint at still deeper evolutionary connections. The suggestions are strong that the programmed polymerizations (translation and nucleic acid repli­ cation) have arisen out of more primitive metabolic interactions. Therefore, what seems called for at this juncture is a general view of polymerization pro­ cesses, one that attempts to relate polymer formation to the full spectrum of metabolic reactions in primi­ tive systems - e. g. the types of polymers arising under primitive conditions; the range of monomer units and chemical linkages involved; whether polymers were formed by monomer or oligomer condensations; chirality constraints; whether the sequences of the aboriginal polymers were random or (simply) ordered (e. g. homopolymers, poly­ mers of alternating sequence, etc. ); the extent to which templating is or is not involved; and oligonucleotide-amino acid interactions. Geological and phylogenetic constraints

time interval during which the evolutionary process could have started. The Earth's crust is now believed to have been initially quite hot, too hot to sustain liquid water. Any water present would have been partitioned between the primitive atmosphere and a semi­ molten crust. There is also geological evidence to suggest that the Archaean oceans were warm. The oldest sedimentary rocks (3800 Ma), although somewhat metamorphosed, give evidence of life at that time; and the better preserved 3500 Ma sedi­ ments give clear evidence of baderial life - showing both fossil stromatolite structures and microfossils (see also Section 1 .2 ). In that stromatolites today are produced by photosynthetic bacteria, principally cyanobacteria (or thermophiles of the Chloroflexus type), photosynthetic bacteria (probably) already existed 3500 Ma. The explosive developments in molecular phylo­ geny over the past decade have revealed a number of important facts: (1 ) the earliest phylogenetic branchings gave rise to three aboriginal lineages, the eubacteria, the archaebacteria and the eukaryo­ tes; (2 ) photosynthesis appears to have arisen (early) within the eubacteria. If so (given the stroma­ tolite evidence), eubacteria already existed at least 3500 Ma, so that the most recent ancestor common to all life lived at a still earlier time - probably far earlier, because of the enormous evolutionary dis­ tances that separate the three classes; (3 ) prokaryotic life (at least) arose in high temperature environ­ ments; (4 ) the ancestral environments were an­ aerobic; and (5 ) the ancestral forms of prokaryotic metabolism may have been autotrophic. Compari­ sons among the (sequences of the) genomes of diverse organisms will ultimately permit us to infer in some detail the nature of the most recent common ancestor of all extant life, and also certain things about still earlier evolutionary stages (see also Section 2 . 1 ) All the evidence to date, then, points to life having arisen quite early in the planet's history, and under thermophilic conditions. .

on the primitive ocean scenario

Knowing when the evolutionary process started is crucial to understanding how it occurred. Con­ ditions during the first few hundred million years of Earth's existence were certainly very different from those occurring 2000 million years later. The current understanding of the geological his­ tory of the Earth, Moon, and other planets, together with recent advances in the biologist's under­ standing of phylogeny, substantially restrict the

Alternatives to the primitive ocean scenario

An important methodological rule of K. Popper is that a new theory should have a greater explanatory power than its predecessors, i. e. it should explain a multitude of facts with a minimum of assumptions. Clearly, today's consensus theory of the origin of life is little more than a highly amended version of the original OparinlHaldane scenario it has replaced - which violates Popper's rule. Further

8

1 Major Events in the History of Life

amendments to the standard scenario are not what is needed; true alternatives to it are. Wachtershauser (1988 ) has proposed one such alternative, which dispenses with the multi-theatre assumption, the ocean repository, heterotrophic origin, and modular self-assembly. This theory, moreover, is sufficiently detailed to make testable assertions regarding the nature and evolution of primitive biochemical pathways. The first organ­ isms are assumed to be truly autotrophic (not hetero­ trophic) - the result of de novo biosynthesis of organic constituents by the uptake of inorganic material (e. g. CO2), and subsequent rearrangement reactions. They are not the products of accidental modular assembly. The theory's central idea is that life began with autocatalytic, metabolic pro­ cesses occurring in an essentially two-dimensional fashion, within organic monolayers anionically bonded to positively charged surfaces of minerals, such as pyrite, and in contact with water at high temperature. Adherence to the mineral surface is not the result of adsorption but of an in situ auto­ trophic growth of organic constituents that acquire their anionic surface bonding in statu nascendi. The concentration of dissolved organic constituents in the water phase is negligible. Hence the process by which a constituent loses its surface bonding is irreversible; detachment is tantamount to dis­ appearance. (In this respect the theory is the op­ posite of Bernal's clay theory, which is based upon adsorption). On these pyrite surfaces large poly­ anionic constituents, with ever stronger surface bonding, are automatically selected - to begin with polyanionic coenzymes, eventually nucleic acids and polypeptides. The primitive system grows by spreading onto vacant surfaces, reproduces by producing its autocatalytic coenzymes, and its evolution is driven by environmentally induced ignitions of new autocatalytic cy cles. The system evolves toward higher complexity, since the ther­ modynamic equilibrium in a surface metabolism would favour synthesis, not degradation (as would occur with solution reactions). High energy phospho-anhydride groups are not required for the formation of covalent bonds. Phosphate groups (whose source is taken to be the mineral substrate) have the sole function of surface bonding. The energy for carbon fixation is provided by the redox process of converting ferrous ions and hydrogen sulphide into pyrite, which is not only a waste product but provides the all-important binding sur­ face for the organic constituents. This initial laminar organism is succeeded by two

further stages. The second stage organisms are semicellular entities still supported by a pyrite sur­ face but having an (autotrophically grown) lipid over-layer, with an internal broth of detached con­ stituents. In this 'bleb' stage a membrane metabo­ lism and a cytosol metabolism appear, first as a supplement to, and later as a substitute for, the aboriginal surface metabolism. Membrane-bound electron transport chains allow the tapping of other redox energy sources and ultimately of light energy. The cytosol metabolism allows the salvaging of detached constituents by catabolic processes and the development of modular modes of synthesis that rely upon energy coupling. Eve�tually hetero­ trophy appears, as a by-product of the catabolic salvage pathways. The cell's genetic machinery develops from surface-metabolic precursors. It produces self-folding enzymes which compete with the mineral surface for bonding the metabolic con­ stituents. In this stage evolution becomes double tracked, an evolution of metabolic pathways and one of the bonding surfaces for their constituents. In the third stage the pyrite support is abandoned and true cellular organisms arise. Since the ocean cannot reasonably function as a reaction pot in which life originated, and its role as a repository is suspect, the question is whether it played any significant role at all in the origin of life. Two types of scenarios exist that make minimal use of the ocean. One is the idea that hydrothermal vents served as the aboriginal environment. Since hydrothermal vents create chemical gradients, a single-theatre vent scenario can be developed that has no need for the ocean repository assumption. How the model would cope with the fact that vents, and so their products, are ephemeral (especially so on an evolutionary time-scale) is unspecified. It was suggested by Woese (1979 ) that evolution began in the primitive atmosphere, at a time when the planet's surface was too hot to sustain liquid water. The early Earth can be pictured as surrounded by vast cloud banks, as Venus is today. The severe weather conditions that must then have existed would have caused large quantities of minerals (dust), from the dry surface, to be swept into the atmosphere. Atmospheric water vapour then con­ densed on the dust, dissolving it (in part). As a consequence, the primitive Earth was enshrouded in clouds of salt water. In addition to containing (possibly high concentrations of) minerals, the droplets in these clouds would accumulate organic compounds, produced by interactions among at­ mospheric gases and other constituents (or with

1.2 Precambrian Evolution compounds produced by thermal reactions on the Earth's surface and swept into the atmosphere). These droplets are natural precursors of cells their surfaces coated with mixtures of the larger organic compounds, their interiors solutions of re­ active (organic and inorganic) compounds. The dif­ ferent layers of the atmosphere would each have characteristic chemistries, the whole being in effect a connected series of chemostats. Droplets (and hydrated dust) offer enormous amounts of surface, and so surface chemistry becomes all important in life's beginnings. As the primitive Earth cooled, its surface would pass from a dry condition, through cycling damp/dry stages, to one where large bodies of (hot) water could accumulate. These major global transitions would bring about major changes in the evolution­ ary course (see above). The cloud setting suggests a single theatre scenario, requiring no repository as­ sumption; it also suggests that major stages in evol­ ution were driven by (were responses to) major changes in the state of the planet. In one sense the origin of life problem today remains what it was in the time of Darwin - one of the great unsolved riddles of science. Yet we have made progress. Through theoretical scrutiny and experimental effort since the nineteen-twenties many of the early naive assumptions have fallen or are falling aside - and there now exist alternative theories. In short, while we do not have a solution, we now have an inkling of the magnitude of the problem.

9

References Bernal, J.D. 1967. The origin of life. World Publishing Co., Cleveland, Ohio. Cairns-Smith, A.G. 1985. Seven clues to the origin of life. Cambridge University Press, Cambridge. Dyson, F.J. 1985. Origins of life. Cambridge University Press, Cambridge. Eigen, M., Gardiner, W., Schuster, P. & Winkler-Oswatitsch, R. 1981. The origin of genetic information. Scientific

American 244, 88-1 18. Fox, S.W. (ed.) 1965. The origins of prebiological systems: and of their molecular structure. Academic Press, New York. Horowitz, N.H. 1945. On the evolution of biochemical syn­ theses. Proceedings of the National Academy of Sciences,

USA 31, 153-157. Katchalsky, A. 1973. Prebiotic synthesis of biopolymers on inorganic templates. Naturwissenschaften 60, 215-220. Miller, S.L. 1953. A production of amino acids under possible primitive earth conditions. Science 117, 528-529. Oparin, A.l. 1938. The origin of life. (Translation of 1936 Russian Edition.) Macmillan, London. Orgel, L.E. 1973. The origins of life: molecules and natural selection. John Wiley & Sons, New York. Urey, H.C. 1951. The origin and development of the earth and other terrestrial planets. Geochimica et Cosmochimica

Acta 1, 209-277. Wachtershauser, G. 1988. Before enzymes and templates: theory of surface metabolism. Microbiological reviews. 52,

452-484. Wald, G. 1964. The origins of life. Proceedings of the National

Academy of Sciences, USA 52, 595-611. Woese, C. R. 1979. A proposal concerning the origin of life on the planet Earth. Journal of Molecular Evolution 13, 95-101.

1.2 Precamb rian Evolution of Prokaryotes and Protists A . H . KNOLL

Introduction

The Phanerozoic Eon, the interval under discussion in most of this volume, encompasses the most recent 13% of our planet's history. A sedimentary record documenting more than 3000 Ma of Archaean and Proterozoic time extends below the base of the Cambrian System, and research conducted over the

past three decades has demonstrated that this entire sweep of history is the proper domain of palaeon­ tology. Stromatolites, microfossils, and geochemical markers provide fragmentary, sometimes frustrat­ ing, but critically important evidence for early evo­ lution. Like younger invertebrate fossils, fossil

1 Major Events in the History of Life

10

prokaryotes and protists must be studied as popu­ lations characterized by a measurable range of morphological variation, reproductive pattern, behavioural orientation, taphonomic features, and distribution within and among sedimentary en­ vironments. Unlike invertebrate fossils, significant questions of metabolism may remain after popu­ lations have been otherwise characterized. The interpretation of early metabolic diversity requires that morphological investigations be supplemented by trace fossil studies (stromatolites and oncolites being the preserved traces of microbial communi­ ties) and geochemical analyses of ancient metabolic and environmental indicators. Geological data must be integrated with information from molecular phylogeny and the comparative physiology of living organisms, and interpreted with a clear appreciation of our incomplete understanding of both living micro-organisms and their geological record.

The Archaean E on: the early diversification of micro-organisms

The age of the earliest palaeobiological record has not changed appreciably in more than 20 years, but the quality of interpretable evidence has improved significantly at decadal intervals. Palaeobiological investigations of Early Archaean rocks have con­ centrated on two successions, the Onverwacht Group of South Africa and the Warrawoona Group, Western Australia. Both sequences are dated at c . 3500 Ma. Both are little-metamorphosed greenstone belt successions characterized by thick mafic and ultramafic lavas, subordinate felsic volcanics, and intercalated sedimentary rocks. Sediments origi-

Fig 1

nated largely as volcaniclastics and chemical pre­ cipitates, including carbonates, but most have been extensively silicified. Stratiform, domal, and colum­ nar to pseudocolumnar stromatolites occur locally in both areas (Byerly et al. 1986 ; Walter in Schopf 1983 ). These structures have generally been inter­ preted as the trace fossils of microbial communities. Although this interpretation is reasonable, no Early Archaean stromatolites are known to contain micro­ fossils. Thus, abiological alternatives must be con­ sidered, and biogenicity defended on the basis of gross morphology and microstructure (Buick et al. 1981 ). Microfossils have also been reported from both groups. Simple carbonaceous spheroids of varying size were reported from several horizons in the Onverwacht and overlying Fig Tree groups during the nineteen-sixties but the biogenicity of many of these structures is open to question. During the nineteen-seventies, several authors reported popu­ lations of spheroidal carbonaceous microstructures that show a number of features more consistent with a biological interpretation. These include a narrow, nearly normal size frequency distribution about a mean diameter of 2 . 5 f! m, clear evidence for binary division, a sedimentary context com­ parable to that of younger, undisputed microfossils, and taphonomic features comparable to younger fossils such as flattened and wrinkled vesicles and the occasional preservation of internal carbon­ aceous contents (Fig. 1K). Rod-like and filamentous microstructures have also been reported from the Swaziland succession, but their antiquity and mode of origin remain subjects for debate. Undoubted filamentous microfossils have re­ cently been described from cherts of the Warra-

Representative Archaean and Proterozoic fossils. A, Gunflilltia (filaments) and Huroniospora (spheroids) in stromatolitic

chert from the Lower Proterozoic Gunflint Iron Formation, Ontario. E, Stromatolites from the Upper Proterozoic Backlundtoppen Formation, Spitsbergen. C, D, Low and high magnification views of a surface-encrusting cyanobacterial population from the Upper Proterozoic Limestone- Dolomite 'Series', central East Greenland - the nested cups are successive extracellular envelopes produced by coccoidal cyanobacteria that jetted upward from the sediment surface, much as morphologically similar populations in peritidal environments of the Bahama Banks do today. E, F, Chroococcalean cyanobacteria from silicified playa lake carbonates of the Upper Proterozoic Bitter Springs Formation, Australia. G, Vase-shaped protist from the Upper Proterozoic Elbobreen Formation, Spitsbergen. H, Low magnification view of oscillatorian cyanobacteria from the Upper Proterozoic Backlundtoppen Formation, Spitsbergen, showing the alternation of vertical and horizontal orientations characteristic of many mat-building populations. I, Acritarch isolated from shales of the Upper Proterozoic Chuar Group, Arizona. J, Endolithic hyellacean cyanobacterium in silicified ooids from the Upper Proterozoic Limestone - Dolomite 'Series', central East Greenland - ooid surface is toward the top of the photograph. K, Spheroidal microstructure from a population showing various stages of binary division, Early Archaean Onverwacht Group, South Africa . L, Large, process-bearing acritarch preserved in chert nodules within a moderately metamorphosed succession of latest Proterozoic age, Prins Karls Forland, Svalbard . Bar

=

30 Ilm for A, 10 cm for B, 400 Ilm for C, 100 Ilm for D, 20 Ilm for E, F and I, 50 Ilm for G, H and J, and 75 Ilm for L.

1 .2 Precambrian Evolution

11

12

1

Major Events in the History of Life

woo na Gro up (Scho pf & Packer 1987), where they o ccur in asso ciatio n with clusters o f sphero idal unicells encased in multiple extracellular envelo pes. These micro fo ssils are mo rpho lo gically similar to extant cyano bacteria, and may be early represen­ tatives o f this gro up; ho wever, that interpretatio n is by no means assured. Even if the fo ssils do represent early cyano bacterial ancesto rs, there is no assurance that they were o xygenic pho to auto tro phs using two pho to systems. In the presence o f H2S, many living blue-greens pho to synthesize ano xygenically using o nly pho to system I, i. e. H2S, H2, o r o rganic mo l­ ecules do nate electro ns, and no O2 is pro duced. Co mparative bio chemistry indicates that this pho to synthetic system evo lved earlier than the cyano bacterial (and higher plant) pathway in which water do nates electro ns. The apparent lo w mo rpho lo gical diversity o f described Early A rchaean micro fo ssils canno t be taken too literally. Studies o f Early Pro tero zo ic assemblages fro m Western A ustralia have demo n­ strated that, as mo rpho lo gically varied assemblages o f fo ssils undergo increasing diagenetic and in­ cipient metamo rphic alteratio n, they beco me ' archaeanized' - i. e. they appear to co nverge mo rpho lo gically o n the simple micro structures fo und in weakly metamo rpho sed Early A rchaean cherts (Kno ll et al. 1988 ). The bio lo gical fixatio n o f CO2 is acco mpanied by a marked fractio natio n o f the stable iso to pes o f 2 carbo n, 1 C and 1 3c . Carbo n iso to pic ratio s in Onverwacht and Warrawoo na carbo nates and kero gens indicate significant fractio natio n between o xidized and reduced species, suggesting an Early A rchaean carbo n cycle fuelled by pho to synthesis, po ssibly under co nditio ns o f elevated Pe0 2. Sulphur isoto pes are likewise fractio nated during dissimilato ry sulphate reductio n, but in co ntrast to carbo n, Early A rchaean sulphur-bearing samples sho w little fractio natio n between sulphides and sulphates. A t t he same time, sedimento lo gical evi­ dence indicates that sulphate was an impo rtant anio n in the water bo dies beneath which bo th the Onverwacht and Warrawoo na beds accumulated. Th is apparent parado x has several po ssible expla­ natio ns: (1 ) it is po ssible that Early A rchaean o ceans co nt ained negligible sulphate co ncentratio ns, and that ro cks co ntaining evidence fo r sulphates in bo th the Onverwacht and the Warrawoo na gro ups accumulated under no n-marine co nditio ns - an explanat io n that is unsatisfacto ry to many geo lo gists familiar with the ro cks; (2 ) it is po ssible that signi­ ficant co ncentratio ns o f sulphate existed in o cea ns

fo r several hundred millio n years befo re pro karyo tes learned to use it - an explanatio n unsatisfacto ry to micro bio lo gists, who no te that bacteria evo lve rap­ idly to explo it no vel substrates; o r (3 ) perhaps almo st all sulphate in po re fluids was reduced bio ­ lo gically to sulphide in an essentially clo sed system with little fractio natio n because o f high ambient temperatures (70°C o r mo re) - a theo ry fo r which the geo lo gical reco rd pro vides little suppo rting evi­ dence. A generally acceptable so lutio n to this pro b­ lem has no t yet been pro po sed. Despit e o utstanding pro blems o f palaeo bio lo gical interpretatio n, it seems clear that 3500 Ma the Earth suppo rted co mplex pro karyo tic eco systems driven by pho to synthesis. Oxygen may have been gener­ ated by Early A rchaean cyano bacteria, but geo ­ chemical evidence indicates that any O2 pro duced was largely co nsumed by the o xidatio n o f o rganic matter, ferro us iro n, and sulphides. A mbient P0 2 appears to have been lo w and physio lo gical path­ ways, co nsequently, anaero bic. Oxide facies iro n fo rmatio n is fo und in Early A rchaean basinal facies, but no t in shallo w vo lcanic platfo rm sequences, pro mpting speculatio n that o xygenic pho to syn­ thesis may have o riginated in ' mid-gyre' enviro n­ ments far fro m sites o f vo lcanic o r sedimentary H2S generatio n. Co mpariso ns o f info rmatio nal macro ­ mo lecules in extant micro -o rganisms independently suggest rapid metabo lic diversificatio n early in evo lutio nary histo ry. Early branching gro ups in bo th the eubacteria and archaebacteria are pre­ do minantly anaero bic, thermo philic, and sulphur­ dependent; several are auto tro phic (Wo ese 1984 ). The search fo r o lder bio lo gical reco rds is limi ted by the paucity o f pre-3500 Ma sedimentary se­ quences. 3800 Ma ro cks fro m Isua, so uthwestern Greenland, co ntain reduced carbo n that is iso ­ to pically fractio nated relative to carbo nates in the same successio n, but the metamo rphism o f these ro cks to amphibo lite grade has o bliterated any un­ ambiguo us indicatio ns o f bio lo gical activity. L ater A rchaean successio ns in A ustralia, A frica, and No rth A merica co ntain diverse stro mato lites, rare micro fo ssils o f cyano bacterial aspect, and lo cal evi­ dence o f unusually stro ng carbo n iso to pe fractio n­ atio n. Mo st o f the iso to pically light kero gens co me fro m no n-marine depo sits, so their interpretatio n in terms o f glo bal co nditio ns is no t straightfo rward; ho wever, it has been suggested \that iso to pically light kero gens fix a minimum age fo r the evo lutio n o f a ero bic methylo tro phy (the metabo lic o xidatio n o f methane o r o ther o ne-carbo n co mpo unds; Hayes in Scho pf 1983 ).

1 .2 Precambrian Evolution The Early Proterozoic Eon: the diversification of aerobes

The modem era of Precambrian palaeontology began in 1954 with the brief description by S. Tyler & E. S. Barghoorn of microfossils preserved in cherts from the 2000 Ma Gunfl int Iron Formation, Canada. Sub­ sequent research has demonstrated that several discrete microfossil assemblages occur in Gunflint rocks. Stromatolitic cherts near the base of the for­ mation contain abundant microfossils preserved as organic, haematitic, or pyritic structures. Although more than a dozen valid species have been described from this facies, two taxa together comprise more than 99% of all individuals (Fig. lA). Gunflintia minuta is a thin (usually 1 -2 !-! m) fila­ mentous sheath that has been compared to both nostocalean cyanobacteria and iron bacteria. Its affinities remain uncertain; locally inflated areas along filaments interpreted as akinetes and hetero­ cysts (distinct cell types produced by nostocalean blue-greens) are probably diagenetic in origin. Small (2 - 15 !-! m) spheroidal fossils assigned to the genus Huroniospora occur in the same beds. The phylogenetic relationships of these populations are also unclear, but their recent interpretation as bac­ terial spores merits serious consideration. Other microfossils in the Gunfl int stromatolitic assem­ blage are uncommon; they include probable iron­ oxidizing bacteria, possible cyanobacteria, and problematica, but no strong candidates for eukaryotic assignment. Although these fossils occur within laminated stromatolitic structures, Gunflintia and Huroniospora populations do not display the orientations charac­ teristic of mat-building micro-organisms in younger rocks. Thus, like their phylogenetic relationships, their ecological interpretation as mat-builders is open to question. Non-stromatolitic Gunfl int assemblages include microbenthos preserved in silicified muds and probable planktic populations. The mud micro­ benthos is dominated by stellate microfossils inter­ preted as iron and manganese oxidizing bacteria, while the apparent planktic forms are 6 - 31 !-! m dia­ meter spheroids of uncertain systematic position. Whatever the taxonomic affinities of Gunfl int microfossils, it is clear that generally similar assem­ blages were widely distributed 2000 Ma. Assem­ blages comparable to Gunflint mud, mat, and plankton fl orules occur in Labrador, the Canadian N orthwest Territories, and two areas in Western Australia (references in Knoll et al. 1988 ). Not all of

13

these occur in iron formations, and several contain microfossils not found in the Gunflint Formation itself. For example, silicified carbonate muds of the Duck Creek Dolom ite, Western Australia, contain septate filaments as much as 63 !-! m in diameter among the largest such fossils known from any Proterozoic formation. Although Gunflint-like as­ semblages are widely distributed in Lower Protero­ zoic formations, they are not the only fossils in rocks of this age. Assemblages from hypersaline peritidal roc ks of the Belcher Supergroup, Hudson Bay, Canada, contain populations that are indis­ tinguishable from cyanobacteria found today in comparable environments (Hofmann 1976 ). Stromatolites are abundant and morphologically diverse in Lower Proterozoic platform carbonates (Walter 1976 ). It is not certain whether the observed increase in stromatolite diversity between the Late Archaean and Early Proterozoic eras refl ects a radi­ ation in mat-building prokaryotes, a preservational consequence of Late Archaean continental crustal growth and stabilization, or both. What may have been the most profound evo­ lutionary changes of the Early Proterozoic Era are events that must be inferred from sedimentological and geochemical data. During the Early Proterozoic, the degree of isotopic fract ionation recorded in sulphur-bearing minerals increased substantially. Detrital uraninite ceased to be a significant con­ stituent of f luviatile and deltaic sediments , while red beds became widespread. Limited data suggest that iron retention in palaeosols developed on mafic parent materials decreased by the end of this interval. Beginning with Preston Cloud, numerous com­ mentators have suggested that these phenomena refl ect a significant increase in the partial pressure of oxygen in the Earth's atmosphere. This has sometimes been interpreted as meaning that the Early Proterozoic atmosphere shifted from reducing to a composition comparable to the present; how­ ever, such a black-and-white view no longer seems tenable. The Archaean (especially the late Archaean) atmosphere undoubtedly contained some molecular oxygen, albeit in low concentrations. At the end of the E arly Proterozoic Era, the atmosphere probably contained only one to a few per cent of present day O2 levels. The difference, however, is metabolically significant; aerobic respiration is possible in the latter atmosphere, but not in the former. Some palaeontological evidence supports the idea of Early Proterozoic aerobic prokaryotes, but clearer insights come from molecular phylogeny and comparative

1 Major Events in the History of Life

14

physiology. In many aer obic physiological path­ ways, oxygen-r equir ing steps ar e appended to an other wise anaer obic ser ies of r eactions (C hapman & 5 chopf in 5 chopf 1983 ). Molecular data, specifically compar isons of nucleotide sequence in 1 65 r ibo­ somal RNA molecules among differ ent living micr o­ or ganisms, suggest that aer obic r espir ation evolved independently in a number of gr oups, most of which ar e fundamentally photoautotr ophic (Woese 1984 ). If one accepts that br oad constr aints on the timing of evolutionary events can be gleaned fr om molecular data, then it can be inferr ed fur ther that the polyphyletic evolution of aer obic pr okar yotes occurr ed dur ing a r elatively br ief per iod following a long per iod of anaer obic evolution (Fig. 2 ). The later Proterozoic Eon: the emergence of protists

Although tr eated last in this chr onological account, the later Pr oter ozoic Eon might have justifiably been discussed fir st, because its palaeobiological r ecor d, especially for the per iod 900 -600 Ma, is far mor e extensive and better pr eser ved than that of ear lier epochs. Near ly 200 Late Pr oter ozoic

o ( Ma)

Anaerobes

A n i m a llPlant associ ated ( Polyphyl e t i c)

Aerobes ( Polyphyletic)

570±20

P

I

,

, I ?

C H

I 4000

I , ,

I I I

Y

3000

A E A

?

I I ?

Endosymbiotic o r i g i n s of m itoc h o n d r i a ( Polyphyletic)

?

I

I I I , ,

Eu karyotic cytosol ancestor I

?

P R O KARYOTES 4600 Fig. 2

Endosymb of p l a s ti ds ( polyphylet i c )

L----- : � :I

2000

2500

N

?

v

,iotic � lI origins

C

A R

Seaweeds

1 000

T E R

o Z o

1 -c e l l ed p rot ists seen in fos s i l reco rd

f;;:J

P

H

�

micr ofossil biotas ar e known fr om sev. en continents (Knoll 1985 ). Envir onmental sampling is far better than for ear lier er as. Thus, it is in later Pr oter ozoic sequences - wher e the r ecor d is cl ear est - that pr inciples of palaeoecological, palaeogeogr aphical, taphonomic, systematic and, hence, evolutionar y inter pr etation can best be established. Late Pr oter ozoic micr ofossil assemblages have been r epor ted fr om silicified car bonates r ep­ resenting a var iety of per itidal depositional en­ vir onments. In situ micr obenthic populations occur in str atifor m str omatolites an d, much less fr e­ quently, in conoidal, domal, or columnar for ms (Fig. 1 C -F, H). Micr obenthos can also be found in silicified micr ites, oncoids, and ooids, as well as in shales and, r ar ely, in unsilicified car bonates. Ther e is a str ong corr elation between facies and assem­ blage composition. Many populations ar e con­ vincingly inter pr eted as cyanobacter ia, although under exceptional cir cumstances bacter ial heter o­ tr ophs can be r ecognized. Less amenable to inter ­ pr etation ar e populations of unor namented 1 0 -20 [tm spher oids that ar e distr ibuted spor adically thr oughout most fossilifer ous r ocks. Although their simple mor phology pr ecludes confident systematic

Summary chart illustrating generalized patterns of prokaryotic and protistan evolution.

PROTI STS

?

1.2 Precambrian Evolu tion classification, some o f these fossils r esemble the cells and cysts of gr een algae and protozoans that occur in moder n micr obial communities of per it idal and hyper saline lake envir onments. J udging fr om their spatial distr ibution within and among facies, other spher oid populations appear to be allo­ chthonous, pr obably planktic, elements. Many Late Pr oter ozoic pr okar yotes differ little in mor phology, development, or behaviour fr om living c yanobacter ial populations found in physical en­ vir onments like those inferr ed for the fossils. For example, endolithic microfossil assemblages found in silicified ooids fr om the 700 -800 Ma Eleonor e Bay Gr oup, East Gr eenland, contain half a dozen discr ete populations which have close moder n counter par ts in present day Bahamian ooid shoals (Fig. In . Late Pr oter ozoic cyanobacter ia appear to be essentially moder n in their diver sity and en­ vir onmental distr ibution. One can hypothesize that the appar ent incr ease in cyanobacter ial diver sity r ecor ded in the Pr oter ozoic as a whole is mainly a function of mor e complete sampling in younger successions; that is, the major featur es of cyano­ bacter ial diversity wer e established dur ing the Ear ly Pr oter ozoic Er a or ear lier . This hypothesis cannot be r ejected on the basis of curr ently available data. The r ecord of other pr okar yotes is less clear , although the pr esence of Late Pr oter ozoic sulphate r educer s, methanogens, methylotr ophs and other bacter ia can be established or inferr ed on the basis of geochemical evidence. Str omatolites pr ovide sedimentar y evidence for the continued wide distr ibution of micr obial mat communities in later Pr oter ozoic envir onments (Fig. lB). It has been suggested that Pr oter ozoic str omatolites changed systematically as a function of age, and that this provides indir ect evidence for Pr oter ozoic cyanobacter ial evolution. Sever al objec­ tions can be r aised against this view: (1 ) the debate over the str atigr aphic distr ibution of str omatolite for ms continues unr esolved - hinder ed by the failur e of many r epor ts to place stromatolites in their pr oper sedimentological per spective and by the absence of a r ational, internationally accepted system of nom enclature; and (2 ) it may well be tr ue that cer tain str omatolites char acter ize par ticular time inter vals, but this does not necessar ily say anything about cyanobacter ial evolution. Differ ­ ences between Ear ly and Late Pr oter ozoic str omato­ lites may as easily r eflect the addition of eukar yotic algae to mat-building communities, tempor al changes in featur es of the physical envir onment (such as C aC03 super satur ation), the evolution of

15

uncalcified metaphytes that outcompeted micr o­ or ganisms for space in cer tain envir onments, or the evolution of meiofaunal gr ade metazoans. Undisputed pr otistan fossils ar e abundant in Upper Pr oterozoic r ocks. Lar ge (up to 2 mm) acr i­ tar chs occur in both silicified car bonates and shales (Fig. 1 1 ); some of these may r epr esent the phycomata of planktic pr asinophyte algae, but the systematic r elationships of most ar e uncer tain. Latest Pr oter o­ zoic cher ts a nd finely laminated shales fr om C hina, A ustr alia, and Svalbar d contain par ticular ly complex for ms, including spiny and pr ocess-bear ing populations (Fig. lL). In their gener al level of mor phological complexity, these r esemble younger Palaeozoic acr itar chs, but the Pr oter ozoic for ms ar e invar iably much lar ger and ar e cer tainly distinct at the specific and, usually, the gener ic level. Recent discover ies in Spitsber gen and Ar ctic C anada demonstr ate that the r ecor d of spinose and pr ocess­ bear ing acr itar chs goes back at least to 800 Ma. Vase-shaped micr ofossils of uncer tain systematic position also occur in Upper Pr oter ozoic shales and car bonates (Fig. I G); in some successions, they ar e among the most abundant fossils pr eserve d. Like fossil pr okar yotes, pr otistan micr ofossils r eflect palaeoenvir onments in their distr ibution, but unlike pr okar yotes, they change systematically thr ough time. Ther efor e, acr itar chs have pr oved useful in at least Late Pr oter ozoic biostr atigr aphy (Vidal & Knoll 1983 ; Hofmann 1987 ). The r ecor d of eukar yotes can be tr aced though time at least back to 1 700 Ma, when both the mor ­ phological and molecular geochemical r ecor ds of pr otists begin (J ackson et al. 1986 ). The r ecor d of metaphytes may be almost as long. Diver se multi­ cellular algae occur in Upper Pr oter ozoic r ocks (Hofmann 1 985 ); with somewhat less confidence, both car bonaceous and tr ace fossil r emains in 1300 - 1400 Ma r ocks can be inter pr eted as sea­ weeds. No unequivocal r emains of metazoans have been descr ibed fr om pr e-Ediacar an deposits. Thus, either seaweeds and animals or iginated at str ikingly differ ent times or , for the fir st half of their histor y, animals must have been tiny, meiofaunal gr ade or ganisms unlikely to sur vive as fossils or pr oduce r ecognizable tr aces. While the palaeobiological tr ail of ear ly eukar ­ yotes curr ently turns cold at about 1 700 Ma, it must be admitted that nucleated cells th at wer e incapable of fossilization or , at least, unlikely to be r ecognized as eukar yotic, almost cer tainly existed ear lier . How much ear lier is unclear . The ancestor s of the eukar­ yotic cytosol (nucleus and cytoplasm) appear to

16

1 Major Events in the History of Life

have aris en early in Earth his tory, either directly from the progenote or later from archaebacterial ances tors . The Early Proterozoic P02 increas e prob­ ably fos tered endos ymbiotic couplings between an­ ces tral cytosols and purple nons ulphur bacteria, leading to the polyphyletic evolution of hetero­ trophic, mitochondria-bearing protis ts . The later acquis ition of endos ymbiotic cyanobacteria res ulted in the origin of eukaryotic algae, again indepen­ dently in s everal lineages . I ndeed, it appears that the plas tids of s ome algal groups are des cended from endos ymbiotic eukaryotic algae, giving s uch organis ms a truly complicated phylogeny.

References Barghoorn, E . 5 . & Tyler, S . M . 1965 . Microorganisms from the GunfIint Chert. Science 147, 563-577. Buick, R . , Dunlop, J . 5 . R . & Groves, D J . 1981 . Stromatolite recognition in ancient rocks: an appraisal of irregularly laminated structures in an Early Archaean chert- barite unit from North Pole, Western Australia. Alcheringa 5,

161-181 . ByerIy, G . R . , Lowe, D . R . & Walsh, M.M. 1986 . Stromatolites from the 3,300-3,500 Myr Swaziland Supergroup, Barberton Mountain Land, South Africa. Nature 319 , 489-

491 . Hofmann, H. J. 1976 . Precambrian microfiora, Belcher Islands, Canada: significance and systematics. Journal of Paleon­

tology 50, 1 040-1073.

A postscript on continuing microbial evolution

It is obvious that protis tan evolution did not grind to a halt at the end of the Proterozoic Eon. I t may be less obvious that continuing divers ification has als o been a characteris tic of Phanerozoic prokar­ yotes . On a broad s cale, maj or features of anaerobic metabolic divers ity were es tablis hed during the Archaean, and aerobic pathways were in place by the Early Proterozoic; however, evolving meta­ phytes and metazoans have furnis hed bacteria with a continuing s uccess ion of novel s ubs trates for metabolis m and enteric environments for coloni­ zation. Throughout Earth's his tory, rates of prokar­ yotic evolution have probably been a function of environmental evolution. F rom the pers pective of prokaryotes , then, the evolving multicellular biota can be viewed as a continually changing s eries of environments . Phanerozoic rates of bacterial evo­ lution may have been low in groups little affected by metazoan evolution, but for the many bacteria that depend directly or indirectly on metazoans , evolutionary rates were probably comparable to thos e of the animals thems elves .

Hofmann, H . ] . 1985 . Precambrian carbonaceous megafossils. In: D . F . Toomey & M.H. Nitecki (eds) Paleoalgology: contemporary research and applications, pp. 20-33. Springer-Verlag, Berlin. Hofmann, H.]. 1987. Precambrian biostratigraphy . Geoscience

Canada 14, 135-154. Jackson, M.] . , Powell, T . G . , Summons, RE. & Sweet, L P . 1986. Hydrocarbon shows and petroleum source rocks in sediments as old as 1 . 7 x 1 09 years. Nature 322, 727-729 . Knoll, A . H . 1985 . The distribution and evolution of microbial life in the Late Proterozoic era. Annual Review of Micro­ biology 39 , 391-417. Knoll, A.H., Strother, P.K. & Rossi, S . 1988 . Distribution and diagenesis of microfossils from the Lower Proterozoic Duck Creek Dolomite, Western Australia. Precambrian

Research 38, 257-279 . Schopf, J . W . (ed . ) 1983. Earth's earliest biosphere: its origin and evolution. Princeton University Press, Princeton. Schopf, J . W . & Packer, B . M . 1987. Early Archean ( 3.3 billion to 3 . 5 bilIion-year-old) microfossils from Warrawoona Group, Australia. Science 237, 70-73. Tyler, S. & Barghoorn, E . 5 . 1954. Occurrence of structurally preserved plants in pre-Cambrian rocks of the Canadian Shield. Science 119, 606-608 . Vidal, G. & Knoll, A . H . 1983. Proterozoic plankton. Memoir of

the Geological Society of America 161, 265-277. WaIter, M . R . (ed. ) 1976 . Stromatolites. Elsevier, Amsterdam . Woese, C R . 1984. Why study evolutionary relationships among bacteria? In: K.H. Schleifer & E. Stackebrandt (eds) Evolution of prokaryotes. FEMS Symposium 29, pp . 1-30. Academic Press, London .

1.3 Precamb rian Metazoans M. A. FEDONKIN

Although palaeontology as a science began more than 200 y ears ago, the first descriptions of Pre­ cambrian animals appeared relatively late, only in the first half of this century . This is explained by the rarity of Precambrian animal fossils. This rarity is due to the absence of mineralized skeletons and possibly because of a low biomass of metazoans in late Precambrian ecosy stems.

developing. The name most commonly used for the terminal Precambrian sy stem is the Vendian. Its ty pe area is the Russian Platform. In the upper half of this sy stem most of the soft- bodied fauna dis­ appears, though some trace fossils continue up to the top of the Vendian along with abundant Vendo­ taenian algae (Metaphy ta) and acritarchs (Sokolov & Ivanovski 1985 ).

Distribution in time and space

Origin of metazoans

Remains of the Precambrian fauna are now known from Australia, Africa, America, Europe, and Asia. The most representative localities are in the Nama Group, Namibia, the Pound Subgroup, South Australia, the Charnian Subgroup, U. K. , the Concepti on Group, Southeastern Newfoundland, the Valdai Series of Podolia, Ukraine, on the Onega Peninsula, and in the Khorbusuonka Series in Northern Yakutia (Glaessner 1984 ; Fedonkin 1987). Several thousand specimens assigned to more than 100 speci es have been found thus far in Pre­ cambrian deposits. Imprints and moulds of soft­ bodi ed ani mals are mainly preserved in terrigenous strata accumulated in marine shallow water en­ vironments. Less ty pically , fossils come from deeper water deposits, in turbidite and carbonate sediments. Unique taphonomic conditions in the Pre­ cambrian, due to a combination of special biotic and abiotic factors, resulted in excellent preservati on of non-skeletal i nvertebrates revealing fine details of their anatomy , i . e. external morphology and, in some cases, i nternal organs. The first unequivocal metazoan fossils appear strati graphically above tillites of the Laplandian (Varangerian) glaciation, which took place approxi­ mately 650 -620 Ma. The maxi mum geographical and stratigraphic distribution of Precambrian Metazoa occurs i n the lower half of the interval between these tillites and the base of the Tommotian Stage of the Lower Cambrian above. This i nterval more or less corresponds to the terminal sy stem of the Precambrian. Concepts of this stratigraphic sy s­ tem, known as the Sinian, Vendian, Ediacarian or Ediacaran accordi ng to different authors, are still

The large number and morphologi cal diversity of Metazoa in the first half of the Vendi an indicate that their phy logeneti c roots continue i nto older pre­ Vendian periods. This si tuation is indirectly sup­ ported by a comparative analy sis of amino acid sequences of globines of living i nvertebrates (Runnegar 1986 ) and by a decrease in the quantity and the diversity of stromatolites which began 1000 Ma and accelerated 700 -800 Ma (Walter and Hey s 1985 ). The possibility cannot be excluded, however, that the decline of stromatolites was promoted not only by Metazoa, which infl uenced, grazed upon and di sturbed bacterial mats and broke the stability of substrate, but by a series of glaciations whi ch took place 850 ± 50 , 740 ± 20 and 650 ± 20 Ma. Little i s known about this stage of Metazoan evolution, but it seems likely that the oldest animal communi ties, including Vendi an ones, were characterized by relatively low di versity i n compari son with Cambrian life. If diversity is consi dered to be a peculi ar mechanism for maintai ning the stabili ty of the biosphere, then the low diversi ty Precambrian biota was rather vulnerable to external abioti c fac­ tors as well as biotic innovations. A low diversity Precambrian fauna could not match the stability of later Metazoan communiti es. The possibility cannot be excluded that as soon as multicellular animals appeared, their communi ties were subjected to radical change, including mass extinctions as they approached the Phanerozoic level of differentiation. General characteristics

Late Precambrian animals have a wi de geographical

17

18

1 Major Events in the History of Life

distributio n with many identical fo rms o ccurring at distant lo calities. This indicates co smo po litanism, weak pro vincialism, and evidently lo w rates o f evo ­ lutio n after a rapid adaptive radiatio n at the begin­ ning o f the Early Vendian transgressio n. Altho ugh the systematics o f Precambrian animals are still pro blematic, o bvio us features include a co nsiderable diversity o f life fo rm and bo dy plan, a pro no unced do minatio n by Co elenterata, a lo w ratio o f the number o f species to that o f phyla, large size (even gigantism in many species, especially amo ng the mo st primitive o rganisms), the presence o f all majo r eco lo gical gro ups, co ncentratio n in shallo w marine enviro nments, a lo w activity o f vagile pre­ dato rs and scavengers, a relatively small bio mass o f infauna in benthic co mmunities, an eco lo gical o rganizatio n into sho rt tro phic chains, an abun­ dance o f suspensio n feeders and detritivo ro us animals, and an absence o f active filter feeders. Systematics

The traditio nal appro ach to the systematic po sitio n o f Precambrian invertebrates is based o n co mpari­ so n with yo unger Palaeo zo ic and even Recent animals (see also Sectio n 5 . 2 . 5 ). Fo r example, G laessner (1984 ) placed Precambrian animals in the fo llo wing taxa: phylum Co elenterata (classes Hydro zo a, Scypho zo a, Co nulata, medusae o f uncer­ tain affinity and pro blematic Petalo namae); phylum Annelida (class Po lychaeta); phylum Arthro po da (superclass Trilo bito mo rpha o r C helicerata o f uncertain class, and superclass C rustacea: class Branchio po da); phyla Po go no pho ra, Echiurida and so me fo rms o f uncertain systematic po sitio n. The classificatio n o f the Precambrian animals within the framewo rk o f living invertebrates pro duces many co ntradictio ns. Therefo re o ther appro aches and principles o f classificatio n have been develo ped. Fo r example, an attempt o f co mparative mo rpho ­ lo gical analysis o f Vendian Radiata and Bilateria has led to different results and a new classificatio n o f the o ldest M etazo a (Fedo nkin 1987), which is o utlined belo w. Radial animals (Radiata) . The co elenterate class C yclo zo a is characterized by a co ncentric bo dy plan, a vast disc-shaped gastral cavity, and a wide distri­ butio n o f metho ds o f asexual repro ductio n. So me fo rms have simple marginal tentacles. The repro ­ ductive o rgans are no t kno wn. This class co ntai ns predo minantly sedentary fo rms, and less co mmo nly animals living at the water-air interface and in

the plankto n. The fo llo wing genera are included: Nemiana (Fig lA), Cyclomedusa, Eoporpita (Fig. lE), Kullingia, Ovatoscutum (Fig. lE), Chondroplon, Medusinites, Ediacaria (Fig. l C ), Tirasiana, Nimbia and Paliella (Fig. 2H). The class Ino rdo zo a unites medusa-like o rgan­ isms with a symmetry o f uncertain o rder, which are characterized by a higher o rganizatio n than the C yclo zo a. Vario us co mplicated systems o f gastro ­ vascular channels, the presence o f repro ductive o rgans (go nads), and the do minance o f medusae in this gro up suppo rt this po int o f view. Asexual repro ­ ductio n is no t typical. The pattern o f gro wth in these animals is unusual co mpared to that in Recent co elenterates: new radial elements (antimeres) are fo rmed freely witho ut any regularity thro ugho ut life. Thus, they increase in number and o rder o f symmetry during o nto geny witho ut restrictio n. The co mbinatio n o f co ncentric and radial symmetry indicates a phylo genetic relatio nship between the Ino rdo zo a and C yclo zo a. The Ino rdo zo a includes Hallidaya, Lorenzinites, Rugoconites, Hiemalora (Fig. 2G ), Elasenia, Evmiaksia, and Pomoria. The class Tr ilo bo zo a is characterized by an un­ usual three-rayed symmetry, which o ccurs o nly as a terato lo gical pheno meno n amo ng recent Co elenter­ ata; amo ng o ther M etazo a it is kno wn o nly as a seco ndary feature. L ike the abo ve mentio ned classes o f Precambrian Co elenterata, representatives of the Trilo bo zo a are characterized by a mo de of gro wth unusual fo r recent Co elenterata. During o nto geny, instead o f co uples o f o ppo site antimeres being fo rmed, three antimeres o r identical radial elements in multiples o f three develo ped simul­ taneo usly. The do minatio n o f medusa life fo rms, co mplicated and regular systems o f gastro vascular channels, and a stable quantity o f repro ductive o rgans, indicate a high level o f o rganizatio n co m­ parable to that o f the Scypho zo a. Ho wever, Trilo bo zo a are characterized by different gro wth and symmetry, and an absence o f a circular channel and o ral aperture. It includes Skinnera, Tribra­ chidium, Albumares (Fig. IF), and Anfesta (Fig. 2D). Conomedusites (Fig. 2F), the o nly sedentary o rgan­ ism having a rather dense co nical theca and a fo ur­ rayed symmetry, is assigned to the class Co nulata. Other meduso ids with the same symmetry are do ubtfully co mpared with scypho zo an meduso ids; these include Ichnusina, Persimedusites and Staurinidia. It is no tewo rthy that as the symmetry o f the Precambrian Co elenterata is reduced, their o rgani­ zatio n beco mes mo re co mplicated: fro m primitive,

1 .3

Fig. 1

Precambrian Metazoans

19

Vendian metazoans. A, Nemiana simplex, x 0.5. B, Ovatoscutum concentricum, x 1. C, Ediacaria flindersi, x 1. D, Charnia x 1 . E, Eoporpita medusa, x 1. F, Albumares brunsae, x 4. Specimens in A and D are from the Khatyspyt Formation, Northern Yakutia, U.5.5.R. Specimens in B, C, E and F are from the Ust - Pinega Formation, southeast of the White Sea region, U.5.5.R.

masoni,

20

1 Major Events in the History of Life

Fig. 2 Vendian metazoans. A, Onega stepanovi, x 5 . B, Dickinsonia costata, x 1. C, Mialsemia semichatovi, x 1. D, Anfesta stankovskii, x 1 . 1. E, Bomakellia kelleri, x 0 . 7. F, Conomedusites lobatus, x 1. G, Hiemalora stellaris, x 1 . H, Paliella patelliformis, x 0 . 7 . 1, Pteridinium nenoxa, x 0.7. Specimens in A - E, G, I are from the Ust-Pinega Formation, southeast of the White Sea

Region, U . S . s . R . The specimen in F is from the Mogilev - Podolsk Series, Ukraine, U . S . s . R . , and the specimen in H is from the Khatyspyt Formation, Northern Yalutia, U . s . s . R .

1 . 3 Precambrian Metazoans dominantly sedentary Cyclozoa with a high order symmetry, through more advanced Inordozoa with a radial symmetry of variable (uncertain) order, to medusoid classes with a stable symmetry and the highest organization (Trilobozoa, Conulata, Scyphozoa). This sequence may reflect the early, pre-Vendian phylogeny of Precambrian Coelenterata. Precambrian colonial organisms are shaped like feathers, combs, fans, and bushes (Ford 1958 ; Glaessner & Wade 1966 ; J enkin & Gehling 1978 ; Anderson & Conway Morris 1982 ). Most forms were fixed to soft sediment by disc-shaped or sausage­ like organs of attachment, but rare, pelagic, freely swimming colonies are also known. The degree of integration and habit of these colonies suggest as­ signm ent to the Coelenterata, but it is impossible to determine their exact systematic position without evidence of the structure of individual polyps and the nature of sclerites or spicules that may have been present in some colonies. Functional differen­ tiation of polyps is not known. The possibility that the colonial organisms are representatives of the same coelenterate classes as the solitary forms can­ not be excluded. Colonial forms include Charnia (Fig. ID), Charniodiscus, Paracharnia, Pteridinium (Fig. 21 ), Rangea, Ramellina, Vaizitsinia, and Ausia. The Petalonamae is a special group of coelenterate grade described by Pfl ug (1970 ) as a group of high taxonomic rank that gave rise to many phyla of invertebrates. Most specialists now consider the Petalonamae to be a group of different, possibly unrelated Coelenterata of uncertain systematic position. Among them is the unusual class E rniet­ tomorpha which includes 27 species and 13 genera. However, some authors consider this diversity to be a taphonomic artifact, and reduce E rniettomorpha to five genera or even to one species, Ernietta plateau­ ensis. This sedentary organism had a multi-layered, sack-shaped body and lived with the base of its body partially buried in soft sediment. Bilateral animals (Bilateria). Among bilaterally sym­ metrical Precambrian animals, very few forms have a smooth, nonsegmented body. These are usually represented by only a few or even single specimens, and their interpretation is doubtful. Two monotypic genera, Vladimissa and Platypholinia, can be com­ pared with the turbellarians (Platyhelminthes). Protechiurus is considered to be the oldest echiurid. The overwhelming maj ority of Precambri an B ilateria have features resembling segmentation or metamerism. This initially suggested comparison

21

with annelids, arthropods, and other articulates. However, some so-called 'segmented' forms have an unusual structure: semisegments of the right and left sides alternate. This symmetry of glide reflection is not typical of younger bilaterians, but is known in the Precambrian among polymerous (consisting of numerous anatomically identical body parts) forms in the Dickinsoniidae as well as among oligomerous (consisting of few similar parts) forms in the Vend omiidae. The leaf-l ike Dickinsonia (Fig. 2B; up to 1 m body size) originally considered a coelenterate, or annelid worm or fl atworm, represents an independent branch of metazoans derived from the Radiata long before other bilaterians. This is indicated by the absence of a definite mouth and anus, an imperfect position of numerous semisegments, and relics of radial symmetry in early ontogeny. Dickinsoniidae could represent a separate class Dipleurozoa in the primitive phylum Proarticulata. The fam ily Ven­ domiidae also probably belongs to this phylum. These animals had a small, elongate discoidal body with a broadly arcuate anterior margin; a wide cephalic area is followed by a small number of segments or alternating sem isegments. The distal ends of the (semi)segments do not always reach the lateral m argins of the ovate fl at body. This family tentatively embraces Vendomia, Onega (Fig. 2A), Praecambridium, and Vendia . True segmented animals resembling annelids and arthropods did live in the Vendian oceans, and some of them can be compared to later Palaeozoic counterparts. For exam ple, Parvancorina has a shield-like, rather soft carapace with a faint mar­ ginal rim and elevated anterolateral and median smooth dorsal ridges. Approximately five pairs of stout anterior appendages are followed by up to twenty pairs of posterior fine appendages. The simi­ larity of Parvancorina to the Palaeozoic arthropods of the Marrellom orpha may indicate that it is close to the ancestors of Crustacea (Glaessner 1984 ). A rather unusual body plan is characteristic of the family Sprigginidae, which includes Spriggina and Marywadea. These animals, generally interpreted as annelids, have a horseshoe- shaped or half-moon­ shaped prostomium that resembles the head shield of primitive trilobites. The body segments, how­ ever, resemble those of rather pri mitive annelids. The same combination of a large head and a rather smooth body with long feather-like lateral append­ ages occurs in Bomakellia (Fig. 2E) and Mialsemia (Fig. 2C) - both united in the family B omakellidae. These animals seem to have had a ri gid carapace.

22

1

Major Events in the History of Life

Their body plan does not correspond to that of any group of living invertebrates. Recently it was sug­ geste d that both the Sprigginidae and Bomakellidae should b e assigned to the special class Paratrilobita, related to the phylum Arthropoda. Vendian - Cambrian evolutionary transition

One of the anomalies in the Precambrian Vendian fauna is an absence of evident ancestors of the important Cambrian invertebrate groups, including Archaeocyatha, Mollusca, Brachiopoda, and Echino­ dermata, all of which appear early in the Lower Cambrian as discrete phyletic lines. The low species diversity a nd prevalence of monotypic genera may indicate a relatively short interval between the rise of these invertebrate groups and their acquisition of the ability to build a skeleton. Skeletalization developed gradually during the Vendian (Section 1 .4 ). The first half of the period saw the appearance of Redkinia spinosa, an annelid­ like animal with chitinoid, comb-like jaws. Chiti­ noid tubes of sabelliditids appear at the same level, as well as the calcareous tubular fossils Cloudina. The end of the Vendian saw a wide distribution of tubular shells, sclerites and conodont-like fo rms. The small sizes and wide geographical distribution of the oldest shelly fossils could indicate that their Precambrian ancestors had small body sizes and a planktic mode of life. Trace fossils show that the majority of the vagile benthos lived in shallow-water marine environ­ ments. Dominant among them were deposit feeders and forms of detritivore which collected small food particles. These animals moved by various peri­ staltic methods. Precambrian trace fossils are not as diverse or deep as later examples. The biomass of Vendian infaunal communities was much smaller even in shallow-water environments. Sedentary epi­ faunal forms of the Vendian period (i. e. mainly primitive groups of coelenterates) were dominantly passive suspension feeders and, more rarely, pre­ dators. Active suspension feeders (filter feeders) are unknown. The activity of vagile predators and scavengers was low, at least in the first half of the Vendian. Coelenterata were domi nant in the plankton and nekton. The end of the Vendian Period was a critical moment in the history of life when biological pro­ cessing of sediments increased greatly and many new groups of invertebrates began to inhab it the sea floor. The body size of infauna, represented mainly by soft-bodied animals, also increas ed

at this time. All these phenomena, as well as the formation of a skeleton in other groups, may be adaptive and reflect increasing predation by vagile animals. Burrowing and the formation of skeletons had extremely important biological and evolution­ ary consequences that are not yet entirely understood by palaeontologists and zoologists. Recently Seilacher (1984 ) offered a new morpho­ logical a nd functional in terpretation of some Precambrian animals. Having noted that the Vendian fauna shows no close affinity with later invertebrates, he inferred that Precambrian organ­ isms do not have Recent analogues and have a unique organization. They are characterized by an extensive body surface, which has developed mainly because of their very complicated relief, and a low body volume by virtue of being relatively flat. The high surface-volume ratio of the body allowed the absorption of oxygen and organic matter dis­ solved in water by diffusion through the body sur­ face. Thus, neither a mouth and digestive organs nor respiratory organs were necessary. No less attractive is an older point of view, that the body of many Precambrian animals was favour­ able for harbouring photosynthesizing endosym­ bionts. This is supported by the leaf-like form of the body of many Vendian organisms, their occurrence in shallow water marine environments within the photic zone, and the large size of many of the most primitive form s. A certain correlation between the presence of algae-endosymbionts and large body size is noted, for example, in recent Cnidaria. The gigcm tism of many Precambrian inve rtebrates is especially striking when compared to the first very small shelly fossils which appear at the end of the Vendian and become numerous in the Tommotian Stage of the Lower Cambrian (Section 1 . 5 ). The larger body size of the Vendian Metazoa may reflect an adaptation of prey animals to in­ creasing predation pressure. The first half of the Vendian was characterized by rapid speciation under the conditions of the vast postglacial trans­ gression of the sea. The fauna rapidly reached its characteristic diversity, and rates of phyletic evo­ lution decreased. This is reflected in the large sizes of populations and the absence of provincialism in many groups. The middle of the Vendian saw a mass extinction of many groups (Section 2 . 13 . 1 ), especially those primitive animals which were characterized by a passive mode of feeding. One possible reason for extinction was the appearance of many small an­ cestors of Cambrian invertebrates, which had better

1 .3 Precambrian Metazoans developed modes of feeding and could considerably impoverish food resources in the pelagic zone. The passive feeding of many Vendian sedentary forms was relatively inefficient and may have led to their extinction. The collection of detritus from the surface of the sediment also became less effective. These circumstances, as well as the increasing population densities and growing predation, could direct natural selection to favour forms that began active colonization of bottom sediment with its new trophic peculiarities. The ecological niche of Vendian sedentary Coelenterata in the shallow marine environment became occupied by active suspension feeders (sponges, archaeocyathids, brachiopods) in the Early Cambrian (see Section 1 . 6 ). Possibly in parallel with the extinction of some groups, there was a decrease in body size in others in the second half of the Vendian. This could explain the sharp impoverishment, if not a gap in the fossil record, of invertebrates of the late Vendian. The decrease of body size may have led to the oligo­ merization of many primitive polymerous forms. This in its turn could have resulted in an increase in the level of organization and/or even in the specialization of some forms. From the middle of the Vendian, the increasing activity of predators and scavengers and the de­ structive activity of burrowin g organisms and perhaps the meiofauna inhibited the preservation of soft-bodied forms. Additionally, bioturbation led to more rapid biological oxidation of soft tissues of buried animals. When comparing the world of the Vendian with that of the Cambrian we are comparing two different categories of fossils. This makes it difficult to analyse the early evolution of invertebrates but to some extent explains the apparent absence of phylo­ genetic connections between the faunas of these two periods. The analysis of body plans of Vendian soft-bodied invertebrates reveals some previously unknown directions of morphological evolution in the Metazoa. The great abundance of Radiata in the Vendian refle cts the predominance of radially­ symmetrical animals of coelenterate grade in the early history of metazoans. The high diversity of symmetries reflects an early radiation of this phylum. The development of more complicated morphologies (i. e. the appearance of more complex systems of gastrovascular channels, reproductive organs, etc. ) while symmetry was reduced suggests an evolution from forms with a symmetry of infinitely

23

high order, through forms with an uncertain multi­ rayed symmetry, to forms with a stable order of symmetry. In the course of coelenterate evolut ion the archaic concentric body plan was replaced essentially by a radial one. The dominance of segmented form s am ong Vendian Bilateria possibly reflects a rel at ionship between processes leading to bilatera l sym metry and to metamerism in the phylogeny of early Metazoa. Bu t these processes did not alwa ys lead to coelomates. Unusual peculiarities of constru ctional morphology (from a neontologica l perspective), for example the plane of symmetry of glide reflection in some of the most primitive Vendian bilaterians, may indicate the early origin of bilateral quasi­ segmented forms from rather archaic R ad ia ta with an axis of symmetry of infinitely high or u ncertain order. The existence of a large quantity of short-live d phylogenetic branches in the Precambrian em pha­ sizes the importance of comparative-m orphological analysis at the Vendian chronological level in order t o discover major directions in the early evolut ion of multicellular animals.

References Anderson, M.M. & Conway Morris, S. 1982. A review, with description of four unusual forms, of the soft-bodied fauna of the Conception and St. John's Group (Late Pre­ cambrian), Avalon Peninsula, Newfoundland. Proceedings

of the Third North American Paleontological Convention 1, 1-8. Fedonkin, M.A. 1987. The non-skeletal fauna of the Vendian and its place in the evolution of metazoans. Nauka, Moscow (in Russian). Ford, T.D. 1958. Precambrian fossils from Charnwood Forest.

Proceedings of the Yorkshire Geological Society 31, 211-217. Glaessner, M.F. 1984. The dawn of animal life. A biohistorical study. Cambridge University Press, Cambridge. Glaessner, M.F. & Wade, M. 1966. The Late Precambrian fossils from Ediacara, South Australia. Palaeontology 9,

599-628. Harrington, M.J. & Moore, R.e. 1956. Dipleurozoa. In : R.e. Moore (ed.) Treatise on invertebrate paleontology. Part F: Coelenterata, pp. 24-27. Geological Society of America, Boulder and University of Kansas Press, Lawrence. Jenkin, R.J.F. & Gehling, J.s. 1 978. A review of the frond-like fossils of the Ediacara assemblage. Records of the South

Australian Museum 17, 347-359. Pflug, H.D. 1970. Zur Fauna der Nama-Schichten in Siidwest Africa. I. Pteridinia, Bau und systematische Zugehorigkeit.

Palaeontographica A134, 226-262. Runnegar, B. 1986. Molecular palaeontology. Palaeontology

29, 1-24. Seilacher, A. 1984 Late Precambrian and Early Cambrian

24

1 Major Events in the History of Life

Metazoa: preservational or real extinctions? In: H . D . Holland & A . F . Trendall (eds) Patterns of change in Earth evolution, pp. 159-168 . Springer-Verlag, Berlin . Sokolov, B . 5 . & Ivanovski, A . B . (eds) 1985 . Vendian System.

Historical- geological and paleontological substantiation. Paleontology, Vol. 1. Nauka, Moscow (in Russian) . Waiter, M . R . & Heys, C . R . 1985. Links between the rise of the Metazoa and the decline of stromatolites. Precambrian

Research 19, 149-174.

1.4 Origin of Hard Parts - Early Skeletal Fossils B . RUNNEGAR & S . BENGTSON

Introduction

Hard parts of organisms appeared almost instan­ taneously in the fossil record at the transition from the Proterozoic to the Phanerozoic. Biomineraliz­ ation (Section 4 . 4 ) may have evolved close in time to that event. Earlier records of biogenic minerals are spurious and involve either v ery small, isolated crystals (magnetite of possible bacterial origin) or carbonate encrustation of cyanobacterial sheaths that may have been induced indirectly by the photosynthetic activities of the organism. The earliest records of hard parts involve all major skeletal materials - calcite, magnesian calcite, aragonite, apatite, and opal. (About 40 minerals are known to be formed by modern organisms (Low enstam & Weiner 1983 ), but many of them are unstable under normal diagenetic conditions and they seldom form structures large or distinct enough to be recognized in the fossil record. ) All major types of skeletons are present - spicules, stiffened walls, shells, sclerites, and physiologically dynamic endoskeletons. The Early Phanerozoic skeleton­ forming biotas (Fig. 1 ) represent practically all major taxa of multicellular organisms known to produce mineralized skeletons today, some groups of biomineralizing protists, and a number of extinct groups of organisms, mostly metazoans (see also Section 5 . 2 . 5 ). The original mineralogy of the various groups of Late Precambrian and Cambrian fossils is not always well known. There are comparatively few studies on the diagenesis of early skeletal fossils. The com­ position of the sk eleton in most groups is only known from their gross mineralogy in various types of rock, or inferentially through comparisons with known related taxa. More detailed information has been derived from petrographic and geochemical studies of fossils and surrounding rocks (e. g. J ames

& Klappa 1983 ), and from studies of replicated crys­

tal morphologies (Runnegar 1985 ). This has been done in only a few cases, however, and further studies are needed. Carbonate fossils

Calcium carbonates, mainly calcite, magnesian cal­ cite, and aragonite, are the most common skeleton­ forming minerals today, and appear to have been dominant already among the first skeletal fossils. Whereas aragonite is unstable in diagenesis and is rarely preserved in the fossi l record, calcite and magnesian calcite may preserve their orig­ inal crystallographic structure given favourable circumstances. The tubular fossil Cloudina (see also Sections 1 . 3 , 5 . 2 . 5 ) is often considered to be the earliest known example of a mineralized skeleton, but its strati­ graphic position is somewhat uncertain, and it is not clear that it significantly predates the earliest more diverse assemblage of skeletal fossils. The tubular skeleton of Cloudina consists of stacked im­ bricating calcareous half-rings, suggesting that it was constructed by a secreting gland of an animal that was able to twist around in its tube. The wall was probably partly organic, stiffened by calcium carbonate impregnations. Other early carbonate tube-building animals include the anabaritids, first occurring in the c . 550 Ma Nemakit-Daldyn assemblage (see Fig. 1 ). Anabaritids attained a wide distribution before their disappearance in the Atdabanian. They were triradially symmetrical - an unusual feature sug­ gesting a possible phylogenetic relationship with triradial metazoans of the Ediacaran fauna - and appear to have been less mobile in their tubes than Cloudina. The original mineralogy of the tubes is

1 .4

25

Origin of Hard Parts

450

500

C-O

sso

PreC-C

Ma

� Calc i u m carbonate � Calcite � Aragon i te

� I 1 IQ22l D

Cal c i u m p h o s p h ate Opal i n e s i l ica Agg l u t i n ated skeleton Tentative range

Fig. 1

Temporal distribution of cIades of biomineralizing and agglutinating organisms in the Late Precambrian to Late Ordovician, compiled from various sources. Precambrian-Cambrian boundary (PreC- C) arbitrarily placed at the appearance of the Protohertzina-Anabarites assemblage and assigned an age of 550 Ma (see also Section 5. 10. 2). Clades defined as groups of taxa that appear to derive their biomineralizing habit from a common ancestor. (A few probably polyphyletic groups, such as 'calcareous tubes', have been retained due to their poorly known phylogeny.)

not known, but apparently ubiquitous recrystal li­ zation suggests that they may hav e been formed of aragonite. The succeeding Cambrian faunas c ontain more div erse types of tubular fossils. Some were cylin­ drical, resembling, for example, protectiv e struc­ tures built by certain modern annelids. Others, in particular the widespread and diverse hyoliths (see also Section 5 . 2 . 5 ), had more obtuse tubes and w ere closed by opercula. They were bilaterally symmetri­ cal animals with a U-shaped gut. The shell mineral was most probably aragonite, and a structure re­ sembling mo lluscan crossed-lame ll ar fabr ic has been observ ed in younger Palaeo zoic members of this group. Aragonitic shells are c haracte ris tic of early mol­ luscs (Runnegar 1985 ). The most pri mitiv e shell structure in Cambrian molluscs seems to hav e con­ sisted of a single layer of spherulitic aragonite prisms beneath an organic periostracum. This ty pe of structure may grow in an inorganic manner, and

the shape of the spherul itic 'prisms' is mould ed by surface forces rather than chemical bonds. These kinds of mineral deposits need not hav e been me­ dia ted by a protein substrate. Nacre ous lining s in prismatic sh ells had appeared by at least the Middle Cambrian and may hav e been present in Earl y Ca mbria n time. The fundamental differenc e between the ara gonitic fibres of spheru­ litic 'prisms' and the flat aragonitic tablets of nacre lies in the difference in the hab it of crystals; in nacre, growth on the (001 ) face is v ery slow, whereas in the fibres it is v ery fast. The result is a layered micr ostructure (nacre) which i s much stronger than fibrous aragonite. M ost of the common molluscan ultrastructures had ev olv ed by the Middle Cambrian. In addition to sp herulitic prismat ic aragonite an d nacre, these included tangentially arranged fibrous aragonite, crossed-lamellar aragonite, and foliated calcite. Various solitary and colonial animals among the earliest skeletal biotas built basal skeletons of

26

1

Major Events in the History of Life

calcium carbonate. Most of these are poorly known. The cup-shaped hydroconozoans and the probably colonial Bija and Labyrinthus may only questionably be referred to the cnidarians (Jell 1983 ). Others, such as Tabulaconus and Cothonion, have been studied in more detail and show certain similarities with corals, but their affinities nevertheless remain in doubt. Undoubted skeleton-forming cnidarians are not known until the Ordovician. The basic structural units in rugose and tabulate coral skel­ etons were spherulitic tufts (trabeculae) formed by fibrous calcite. Modem scleractinian corals form similar structures of aragonite fibres. As with the spherulitic 'prisms' of mollusc shells, the process of formation appears to involve little matrix-mediated control of crystal shape. However, nucleation of the fibrous trabeculae may be under more direct biochemical control. The sponge-like archaeocyathans constructed a supporting skeleton typically shaped like a double­ walled perforated cup. They are preserved as micro­ granular calcite, interpreted as representing original magnesian calcite (James & Klappa 1983 ). Calcium carbonate (aragonite or calcite) skeletons are also formed by several groups of sponges ('sclero­ sponges' and 'sphinctozoans') from the Middle Cambrian until the Recent (Vacelet 1985 ). The more common type of sponge mineralization is, however, the spicular skeleton (see below). All the skeleton types described above exhibit incremental growth, which occurs by addition of material to earlier formed growth stages. This type of growth puts strong geometrical constraints on morphology. Ways of avoiding this problem are : (1 ) periodical moulting of exoskeleton; or (2 ) con­ tinuous construction and destruction of the mineral phase by intimately associated living tissue. Trilobites, common in Cambrian rocks from the Atdabanian (c. 540 Ma; Fig. 1), are an example of animals that periodically moulted their exo­ skeletons . These were of calcitic composition and often show well-preserved crystallographic fabrics in their mineralized cuticle. Other examples are the coeloscleritophorans, uniquely Cambrian organisms with a complex exoskeleton consisting of hollow carbonate sclerites with a basal opening. Their orig­ inal mineralogy has not been definitely established, but the ubiquitous recrystallization and occasion­ ally preserved fibrous structure suggest that they were aragonitic. Echinoderms, first appearing in the Atdabanian and undergoing their first substantive radiation in the Middle Cambrian, developed a calcium

carbonate endoskeleton in which there was close interaction of mineral and living tissue. Modem echinoderms construct their skeletons of a mesh­ work (stereom) of almost pure magnesian calcite, in which each individual skeletal component is part of a large single crystal. All fossil echinoderms, in­ cluding the Cambrian ones, appear to have had an identical structure. Spicules - mineralized elements formed within living tissues - are widely distributed among Recent organisms. Spicules of magnesian calcite are characteristic of calcareous sponges and octocorals. In both groups the spicules are formed by special­ ized sclerocytes, sometimes originating intracellu­ larly and only later erupting from the cell membrane to be further enlarged by enveloping sclerocytes. Sponge spicules grow in crystallographic continuity, so that each spicule behaves optically as a single crystal of calcite. By contrast, octocoral spicules typically are composed of smaller acicular crystals. As the echinoderm plates, sponge and octocoral spicules are made of magnesian calcite, it has been suggested that magnesium is used to shape the crystals by selectively poisoning appropriate parts of the lattice (O'Neill 1981 ). Calcitic sponge spic­ ules have been found in the late Atdabanian (c. 535 Ma, Fig. 1 ), and possible octocoral spicules also appear in beds of the same age. Undoubted spi­ cules of octocorals are known from the Silurian. The fossil sponge and octocoral spicules have the same crystallographic properties as their modem counterparts. Although fossil spicules of various origins are common, they are rarely dealt with in scientific literature because they tend to be disarticulated and therefore difficult to identify taxonomically. Some spicular skeletons may fuse to form frameworks, as in hexactinellids, 'lithistid' demo sponges, and 'pharetronid' calcareous sponges, or the axial skel­ etons of pennatulacean and a few alcyonarian octo­ corals. Such structures are rare in the early history of these groups. Fossils resembling calcified cyanobacteria became common in the Early Cambrian. One group of such organisms, the helically coiled filamentous Obru­ chevella, is present as uncalcified filaments in rocks of Vendian age, but is frequently calcified after the beginning of the Cambrian. Calcified cyanobacteria have their mucilagenous sheaths impregnated with crystals, perhaps as a by-product of the photosyn­ thetic removal of CO2 from the water in which they lived (Riding 1977 ). Fossils that may be true cal­ carous algae occur in the c. 550 Ma Nemakit - Daldyn

1 .4

Origin of Hard Parts

beds of the northern Siberian Platform . More con­ vincing examples are first known from the Middle Cambrian. Phosphatic fossils

As a skeleton-forming mineral, apatite occurs today only in inarticulate brachiopods and vertebrates . Some recent organisms are also known t o produce amorphous calcium phosphate that may be crystal­ lized later into apatite . Among the earliest skeletal organisms, however, calcium phosphate appears to have been more widespread . Tubular fossils of phosphatic composition are a common constituent of Cambrian faunas . Most of them are referred to as hyolithelminths . The fine structure of hyolithelminth tubes has not been suf­ ficiently studied, but they appear to have grown incrementally by addition of lamellae . At least in some forms a systematic change in the orientation of fibrous elements in adjacent lamellae occurs, pro­ ducing a force-resistant structure similar to that of arthropod cuticles . The phosphatic tubes of the paiutiids had longitudinal septum-like structures on the inner surfaces . Conulariids had distinctly four-faceted cones built up of transverse phosphatic rods set in a flexible integument. Phosphatic conchs or shells were also widespread . In addition to phosphatic inarticulate brachiopods, there are also a number of problematic phosphatic shells, such as Mobergella and related fossils, char­ acterized by regularly placed paired muscle scars and a usually flattened shape . The brachiopods include a number of phosphate- and carbonate­ shelled clades, many of which were short-lived . One characteristic and diverse Cambrian group is the tommotiids - multisclerite-bearing animals presumably covered with more or less twisted coni­ cal sclerites built up of phosphatic growth lamellae . They vary in skeletal organization from the ir­ regularly shaped and frequently fused sclerites of Eccentrotheca to the highly organized scleritomes of Camenella and Tannuolina, in which each of the two asymmetric sclerite types had its mirror-image counterpart . Examples of periodically moulted exoskeletons of calcium phosphate are rare, but the valves of the ostracode-like bradoriids are commonly preserved as phosphate . Although some of them appear to have been flexible, they were most probably im­ pregnated to varying degrees with apatite crystal­ lites. Like most arthropod skeletons, they did not grow by accretion, but were periodically shed.

27

Whether or not the ecdysis involved resorption of mineral matter is not known, but resorption may explain the common occurrence of collapsed or buckled valves. The problematic fossil Microdictyon formed plate­ like structures with a more or less regularly hexag­ onal network of holes and intervening nodes. They were constructed of two or three distinct layers of apatite and show no evidence of incremental growth . Vertebrates, similar to echinoderms, have a plastic mode of skeleton formation as a result of a constant physiological exchange between mineral­ ized and cellular tissues . The phosphatic bone of vertebrates is intimately associated with fibrillar collagen, which does not seem to be the case in other phosphatic skeletons . Although undoubted vertebrate remains are not known until the Ordovician, certain Cambrian phosphatic fossils show a fine structure suggesting association with fibrous organic matter that may be homologous with vertebrate collagen . The small button-shaped sclerites o f the utah­ phosphans consist of a thin dense apatite layer covering a porous core; the latter has fine tubules or fibrils perpendicular to the lower surface . The 'buttons' are more or less densely set in an integu­ ment that is impregnated with smaller apatitic crys­ tallites. The tooth-shaped conodonts had a fibrous organic matrix in which the apatite crystallites were embedded (Szaniawski 1987) . In both these cases, a chordate affinity has been proposed using partly independent lines of evidence . Other suggested biomineralizing chordates (Palaeobotryllus, Ana to­ lepis) are even more problematic in their inter­ pretation. There are further examples of exclusively Cambrian fossils of phosphatic composition and unknown systematic affinity. Some of these are spine- or tooth-shaped objects, possibly reflecting the fact that apatite is a hard mineral suitable for the construction of wear-resistant structures . Siliceous fossils

Because of its non-crystalline, isotropic nature and intracellular method of formation, opal (a mineral gel consisting of packed spheres of hydrated silica) has had limited potential as a skeletal material ex­ cept in very small organisms . It is most widespread among protists . The only metazoans known to form it are hexactinellid sponges and demosponges, which use it for spicule formation . Most biogenic

28

1 Major Events in the History of Life

opal formed today is either dissolved in the water column before it is incorporated in the sediment or dissolved during early diagenesis, but under certain circumstances opaline skeletons may be preserved, usually as microcrystalline quartz or replacements by other minerals. The distribution of opal among the earliest skel­ etal fossils differs significantly from that of calcium carbonates and phosphates . Only four groups of silica-producing organisms are known from the time period under consideration (Fig . 1), hexacti­ nellids, demosponges, radiolarians, and chryso­ phytes(?) . All appeared during the Early Cambrian and all are still living . Whether this apparent im­ mortality of opal-producing lineages is a chance effect due to the small number of clades involved, or whether it has a more profound meaning, the pat­ tern differs considerably from that seen in the car­ bonate and phosphatic groups . In the latter two, the Cambrian radiation appears to have produced a large number of taxa of which only a few survived . Early history of skeletal biomineralization

Present knowledge of the fossil record confirms that mineralized skeletons of many different kinds and composition appeared very rapidly in a number of clades at the beginning of the Phanerozoic . Analysis of the precise pattern is still difficult, because in many cases the original mineralogy is insufficiently known and the taxonomic understanding of the various enigmatic early skeletal fossils is incomplete (see also Section 5 . 2 . 5 ). It is therefore difficult to know how many clades developed the ability to form mineral skeletons at this time . It seems clear, however, that this ability evolved independently a number of times. A current and widely held view is that those organisms that used phosphate rather than car­ bonate or silica were the first to diversify. Phos­ phate has been stated to be the dominant or even exclusive mineral of the earliest skeletal faunas . A phosphate - carbonate transition is said to have oc­ curred within clades such as the Ostracoda, Brachio­ poda, and Cnidaria, but also by the replacement through extinction of organisms with phosphatic skeletons by organisms with carbonate hard parts . Aragonitic materials are also postulated to have replaced calcitic ones throughout the remainder of the Phanerozoic. Available data, including the pattern of distri­ bution of clades of different biomineralizing habits through time (Figs 1, 2 ) and the phylogeny within

30 .-----�

'" QJ "'Cl '"

U

DO c

20

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QJ C

P h os p h ate s k e l etons

E tu

10

.D

E

:::J Z

S i l ica skeletons

O +-----��---.----r_--._--� 580

560

540

520

500

480

M i l l io n s of years ago Fig. 2 Cumulative curves of appearance of clades presumed to have independently evolved a biomineralizing habit. Based on the same data as Fig. 1 .

these clades, do not appear to support such views . 1 The relative amount of phosphate versus car­ bonate bound in biominerals in the Cambrian has been exaggerated by sampling biases (most early skeletal fossils are of millimetre size, and chemical extraction of microfossils is more likely to destroy carbonates than phosphates) and unrecognized cases of secondary phosphatization (the Cambrian was a time of extensive deposition of phosphatic sediments) . 2 Whereas phosphate skeletons were certainly more widely distributed among different clades in the Early Cambrian than they are today, the same may be said about carbonate ones. Among the clades shown in Fig. 1, 42% of the carbonate skel­ etons survive until the present, as compared to 25% of the phosphatic ones (protoconodonts are regarded as chaetognaths with mineralized grasping spines) . Both categories include clades that are today very successful and diverse. Thus the restriction of phosphate minerals to two major clades today may simply be the result of the different evolutionary success of various early lineages. Nothing in the history of vertebrates suggests that their skeletal mineralogy puts them at an evolutionary disadvan­ tage, and there is no reason to assume that the shell mineral was the particular factor that decided the survival of each of the early lineages. 3 The quoted examples of phylogenetic transition from phosphate to carbonate, or from aragonite to

1 .4

Origin of Hard Parts

calcite, appear to be suspect. For example, a sug­ gested evolutionary succession from phosphate to carbonate hard parts within the cnidarians depends upon the dubious taxonomic decision to place the extinct conulariids within the Cnidaria. The pro­ posed secondary origin of carbonate brachiopods from phosphate ones and the derivation of carbon­ ate ostracodes from pre-existing phosphate forms have the me rit of linking groups that are clearly closely related, but the proposal of a mineralogical transition is nevertheless weakly founded. In neither case has a strict phylogenetic analysis been able to demonstrate that the carbonate forms are in fact derived from the phosphate ones. The Early Phanerozoic radiation cannot be seen j ust as a radiation of biomineralizing taxa. The trace fossil record shows a similar rapid diversification of burrowing habits in non-biomineralizing organ­ isms, and the appearance at the same time of resist­ ant organic structures and agglutinating tubular fossils shows that the key event is not biomineral­ ization as such (see also S ection 1 .5) . To a certain extent, the appearance of mineralized skeletons may be seen as one of many aspects of the early radiation of multicellular organisms. Nevertheless, the apparent absence of biominerals in the Edia­ caran fauna and the nearly simultaneous 'skeletal­ ization' of cyanobacteria (notwithstanding reports of earlier sporadic cases of mineralized cyanobac­ terial sheaths), algae, heterotrophic protists (fora­ miniferans and radiolarians), and metazoans, seems to call for specific explanations. Attempts to explain the appearance of skeletons have often foundered on lack of universality. For example, models involving calcium availability or regulation do not explain the simultaneous appear­ ance of opaline skeletons, and the proposal that biomineralization began as a phosphate-excreting process at a time of high phosphate availability is not consistent with the pattern of appearance of v arious biominerals as discussed above. Models based on increasing P02 may have more explanatory power, as an increasing availability of oxygen would have made it easier for organisms to form skeletal minerals and proteins, and made outer mineralized skeletons less of a respiratory disad-

29

vantage. (There is a general but not perfect corre­ lation between distribution of mineralized skeletons and oxygen levels in modern marine faunas. ) A synecologically based explanation is that bio­ mineralization in animals and plants primarily arose in response to selection pressu res induced by grazers and predators. No evidence of grazers or predators is known from the Ediacaran fauna, whereas the first probable macrophagous predators (protoconodonts) appear with the first diverse skel­ etal biotas. Al though the various types of skeletons in the early Phanerozoic biota often had complex functions, most of them would have had the advan­ tage of at least passively deterring predators or grazers. S uch an explanation stresses the view of the early evolution of skeletons as a complex event, integrated with other aspects of the rapid biotic diversification at this period. It is not in conflict with physiologically and geochemically based models explaining how biomineralization became possible in the first place. References James, N . P . & Klappa, C . F . 1983. Petrogenesis of Early Cambrian reef limestones, Labrador, Canada. Journal of

Sedimentary Petrology 53, 1051-1096 . Jell, J . 5 . 1983. Cambrian cnidarians with mineralized skel­ etons . Palaeontographica Americana 54, 105 - 1 09 . Lowenstam, H . A . & Weiner, S. 1983. Mineralization b y or­ ganisms and the evolution of biomineralization . In: P . Westbroek & E . W . d e Jong (eds) Biomineralization and biological metal accumulation, pp . 191-203. Reidel, Dordrecht. O'Neill, P . L . 1981 . Polycrystalline echinoderm calcite and its fracture mechanics. Science 213, 646-648. Riding, R. 1977. Calcified Plectonema (blue-green algae), a Recent example of Girvanella from Aldabra Atoll. Palae­

ontology 20, 33- 46 . Runnegar, B . 1985 . Shell microstructure o f Cambrian molluscs replicated by calcite. Alcheringa 9, 245-257. Szaniawski, H. 1987. Preliminary structural comparisons of protoconodont, paraconodont, and euconodont elements. In: R . J . Aldridge (ed. ) Palaeobiology of conodonts, pp. 3547. Ellis Horwood, Chichester. Vacelet, J. 1985 . Coralline sponges and the evolution of the Porifera. In : S. Conway Morris, J . D . George, R. Gibson & H . M . Platt (eds) The origins and relationships of lower invertebrates. Systematics Association Special Volume 28, pp . 1-13. Oxford University Press, Oxford .

1.5 Late Precamb rian - Early Cambrian Metazoan Diversification S . C O N WA Y M O R R I S

Introduction

on pre-Ediacaran metazoans, much of it ques­ tionable . The second section then addresses the outlines of the adaptive radiation that is marked by the Ediacaran faunas and the succeeding Cambrian biotas .

Life on this planet is customarily divided into six kingdoms, the prokaryotic archaebacteria and eubacteria, and the four eukaryotic kingdoms of protoctistans, fungi, plants, and metazoans. Because the multicellular metazoans had their origins in unicellular eukaryotic ancestors, in principle the identification of such an organism in the fossil record would constrain the time of appearance of the metazoans . However, even the recognition of the first eukaryotes has proved problematic . It has been customary to regard eukaryotes as being de­ rived from prokaryotes, and given the profound differences between the two cell types such a dis­ tinction might seem to be readily identifiable in the fossil record. However, even these critical characters (e . g . presence of nucleus, cell wall composition) fail to survive fossilization, and the only guide is rela­ tive cell size . Thus, the search for the earliest eukaryotes has concentrated on evidence for either relatively large unicells (see also Section 1 .2) or, better, a more com­ plex multicellular organism, perhaps even with differentiated tissues . In terms of the former cri­ terion, the appearance of large cells in sediments dated at approximately 1300 - 1400 Ma is generally taken as the first reliable indication of eukaryotes . In similar aged strata, fossils composed o f large carbonaceous films probably represent multicellular protoctistans, perhaps brown algae . Nevertheless, given the overlap in cell diameters between eukar­ yotes and prokaryotes, it is not impossible that some cellular remains from yet older sediments are eukaryotes masquerading as prokaryotes . Given these problems, i t i s necessary to review first the generally agreed bench-marks leading to the appearance of metazoans . The earliest definitive metazoans are taken as the Ediacaran faunas (Glaessner 1984) that span the interval c. 550- 620 Ma . Allowing for considerable uncertainties the earliest eukaryotes may be as old as 1600 Ma, allowing a possible 1000 Ma for the development of metazoans. This article, therefore, is divided into two sections . the first reviews such slender evidence as is available

Pre-Ediacaran metazoans

The most compelling pre-Ediacaran evidence would be soft-bodied remains. Recently, structures inter­ preted as worms (Sun et al . 1986) have been reported from Northern China (Anhui and Liaoning prov­ inces) . In overall form some of these carbonaceous structures, known as Sinosabellidites and Pro to­ arenicola are very similar to a sausage-like mega­ scopic Precambrian alga known as Tawuia, but they differ in possessing fine annulations. Another sup­ posed worm, referred to as Pararenicola, also pos­ sesses annulations, but is somewhat smaller and stouter than Sinosabellidites . Nevertheless, their identification as metazoans is otherwise equivocal, not least because neither internal structures, such as a gut trace, nor cephalization are recognizable . In particular, claims for a so-called proboscis in Para­ renicola and Protoarenicola are dubious . Moreover, the quoted dates of between 850 and 740 Ma are based on questionable radiometric determinations and correlations with other regions in China, and the pre-Ediacaran status of these fossils is still open to doubt. With regard to trace fossils from pre-Ediacaran strata, there are numerous claims, but few have won acceptance . Supposed metazoan traces from the Medicine Peak Quartzite of Wyoming (Kauffman & Steidtmann 1981), dated at c. 2000 2400 Ma are remarkable in view of the current consensus that the seas were colonized by nothing higher than cyanobacterial mats . Another widely quoted example is a possible feeding trace (Brook­ sella canyonensis) from the Grand Canyon . This is ostensibly from the 1 100- 1300 Ma old Grand Canyon Series, but renewed searches appear to have been unsuccessful . While other specimens from a wide variety of localities provide a seemingly 30

1 .5

Metazoan Diversification

from a wide variety of localities provide a seemingly impressive roster of evidence for trace fossils, in nearly every case unresolved doubts remain . Even if some pre-Ediacaran traces prove genuine, their general scarcity is difficult to explain unless extrinsic factors (e . g . oxygen levels) prohibited the wide­ scale expansion of macroscopic metazoans into an effectively empty ecospace . While these relatively large trace fossils continue, therefore, to excite scepticism, it may be that more convincing evidence could be found at a micro­ scopic level . For example, possible faecal pellets have been reported from the c. 900 Ma Zilmerdak 'Series' of the Urals (Glaessner 1984), which, if con­ firmed, which, would indicate a grade of organiz­ ation above that of the turbellarians . Clearly, a more extensive survey in suitable lithologies is required . In particular, ultrastructural studies of sediments may show features diagnostic of bioturbation. For example, documentation of grain orientation and cation concentrations (e . g . iron, aluminium) around undoubted Phanerozoic trace fossils suggests a possible approach to establishing the biogenicity of some Proterozoic examples (Harding & Risk 1986) . Moreover, cherts that evidently formed at a very early stage of diagenesis, from the c. 700 Ma Doushantuo Formation in the Yangtze Gorges of Hubei Province, China, preserve narrow burrowlike structures that may represent the activities of a meiofauna. While the Precambrian fossil record is dominated by stromatolites, it has long been realized that they undergo a decline in diversity during the late Pre­ cambrian (see Fig . 2) . A recent reanalysis of the data (WaIter & Heys 1985) indicates that, in terms of both relative abundance and diversity, stromatolites began to decline in quiet, subtidal environments (where coniform varieties were especially abundant) from about 1000 Ma. This trend was established also in intertidal environments from c. 800 Ma, so that stromatolites were relatively unimportant by the beginning of the Cambrian. The traditional explanation links this pattern to the rise of grazing metazoans whose activities were detrimental to the formation of the microbial mats . Thus, the initial dip in stromatolite diversity at 1000 Ma may herald the rise of primitive grazers, while the accelerating process of decline after c. 800 Ma could represent the widespread distribution of metazoans . How­ ever, the development of disrupted stromatolitic fabrics (a thrombolitic texture) that may be a result of extensive burrowing by metazoans, only appears in the Cambrian. Further indirect evidence for the evolution of

31

metazoans at least one billion years ago comes from molecular studies . If it is demonstrated that the substitution of either nucleotides in nucleic acid chains or amino acids in polypeptides is stochasti­ cally constant and occurs at a known rate, then the differences between the sequences in any species pair should indicate their time of divergence . Using this assumption of the so-called molecular clock, existing data on haemoglobins (a group with a substitution rate that is appropriate for the time­ scales involved) have been used to suggest that the metazoans evolved between c. 800 and 1000 Ma. A related approach utilizes SS ribosomal RNA se­ quences, and such comparisons (Hori & Osawa 1987) suggest that Mesozoa might be the most primi­ tive metazoans (if they are not derived indepen­ dently from protoctistans) . Moreover, although the Mesozoa may have arisen before 1000 Ma, other metazoans such as the turbellarians and nematodes have divergence points at only c. 700 Ma . Ediacaran faunas

The evidence for pre-Ediacaran metazoans is mounting, but the view that the fossil record indi­ cates no metazoan older than c. 600 Ma is still respectable and it is the Ediacaran faunas that provide our first useful glimpse of metazoan evol­ ution (Glaessner 1984; Conway Morris 1985; see also Section 1 .3). Such faunas were described from Namibia, at that time Deutsch Sud-West Afrika, before the Second World War, and shortly after­ wards in Australia. At first regarded as Cambrian, their persistent occurrence beneath abundant shelly fossils soon led them to be consigned to the Pre­ cambrian, and continuing reports from numerous localities around the world have confirmed this observation. Until recently these faunas have been dated at c. 620- 680 Ma, with some claims of even 800 Ma. However, recent radiometric dating has cast major doubt on these estimates. High resolution uranium - lead dating of zircons from an ash fall that entombed an Ediacaran assemblage in South­ east Newfoundland (Fig. 1) yields a date of c. 565 Ma . Even so, the age range of the Ediacaran faunas may be considerable, and a span of c. 550- 620 Ma may not be unrealistic. The Ediacaran faunas are reviewed elsewhere (Section 1 . 3), and only a general survey in the present context is required . At present, there seem to be two broad assemblages. There are those of a shallow­ water type that are superbly represented in, the Flinders Ranges of South Australia, including the

32

1 Major Events in the History of Life

Fig. l

Ediacaran fossils from the Mistaken Point Formation (Conception Group) of Southeast Newfoundland, Avalon Peninsula. A, Pennatuloid with hold-fast. B, Pectinate organism. C, Stellate organism. D, Bedding plane with spindle organisms and medusoids. E, Branching organism with hold-fast. F, Pennatuloid with hold-fast and medusoid. Diameter of coin 23 mm.

Ediacaran Hills, and the closely similar fauna from the White Sea of northern U . S . 5 . R . In contrast, the faunas of the A valon Peninsula of southeast New­ foundland, which may be referred to as the Mistaken Point assemblage (Fig . 1), in reference to the spec­ tacular locality near Cape Race, appear to represent a deeper-water facies . Similar occurrences in Charnwood Forest, U.K. are one of the many lines of evidence that in the early Phanerozoic this area was joined to the Avalon area on one side of the Iapetus ocean . Possibly deeper-water faunas may

also occur in the Flinders Range, but as yet only preliminary reports are available . Despite the range of environments inhabited by these Ediacaran assemblages, they show several characters in common . Most typical are forms that the majority of workers would ascribe to the cnidarians . These include medusoids (Fig. ID, F), some of which may be placed with reasonable con­ fidence in cubomedusoids, chrondrophores, and perhaps scyphozoans . However, other jellyfish have a highly characteristic three-fold symmetry

1 .5

Metazoan Diversification

that finds no parallel amongst living cnidarians. Yet others lack sufficient characters to be assigned with confidence to any group . In addition, stalked forms with an expanded leaf-like body arising from a central rachis (Fig . lA, F) invite comparisons with the pennatulaceans (the sea-pens) . However, these similarities become increasingly tenuous amongst a variety of other foliate to bag-shaped organisms, and their cnidarian affinity is more questionable . Other organisms include a possible worm, the sheet­ like Dickinsonia, a medley of arthropod-like forms, and a possible echinoderm with penta-radial symmetry (Gehling 1987) . Although the Mistaken Point assemblages evi­ dently owe their preservation in most instances to being overwhelmed by volcanic ash, in many other cases the occurrences of these soft-bodied meta­ zoans as sandstone impressions above silts tone in­ tervals are difficult to explain, given the absence of such preservation in younger clastics . The problem is compounded by abundant trace fossils in some Ediacaran assemblages, most typically simple sinu­ ous trails, that cannot be linked to the activities of any of the known body fossils . It seems necessary to invoke a contrast between entirely soft-bodied organisms, such as the trace-producing worms that were possibly largely infaunal, and those with a tougher integument, many either epifaunal or pelagic and coming to rest on the sea-floor prior to burial . It was only this latter group that was suf­ ficiently tough to take impressions when immured by sediment. However, the explanation has not won universal approval. In a sweeping reappraisal Seilacher (1989) proposed that the Ediacaran organ­ isms represent an entirely separate group, possibly a distinct kingdom, that owe their preservation to a unique composition consisting of a sac-like body with a tough integument. While Seilacher has high­ lighted the taphonomic problems posed by this preservation, his ingenious proposal seems to be oversimplified and, while perhaps applicable to some of the sac-like ernietiids (see also Section 1 . 3) and Pteridinium, is difficult to reconcile with the bulk of the biota . Whatever disagreements surround the biological affinities of the Ediacaran fauna, it is clear that they lacked hard skeletal material, the widespread ap­ pearance of which was to usher in the Cambrian some 20 Ma later . However, one notable exception demands comment. In Namibia carbonate units, intercalated with clastics containing Ediacaran fossils, yield calcareous tubes referred to as Cloudina (Grant 1990) (see also Section 1 .4) . The tubes are

33

double walled with connecting partitions that give a cone-in-cone appearance, although the exact mode of secretion is not clear . There is evidence that originally the walls contained substantial amounts of organic matter, and this helps to fuel the specu­ lation that the origin of skeletal hard parts was as separate spicules or granules embedded in an organic matrix . The facies contrast in Namibia between the clastics bearing the Ediacaran fauna and the carbonates with Cloudina emphasizes the need for taphonomic judgements concerning orig­ inal faunal distribution . However, occurrence of Ediacaran faunas in dolomites in northern Siberia demonstrates that preservation is not governed simply by lithology . The role of the Ediacaran faunas in determining the origins of the Cambrian fauna at present is enigmatic. With the possible exception of the arthropod- and echinoderm-like forms, existing reports would indicate little continuity with either the shelly faunas or soft-bodied Burgess Shale-type assemblages . Descriptions of new finds from Siberia and Australia may go some way towards alleviating the problem, and it is likely that many of the putative ancestors are represented either by the unknown trace makers or animals too small to be preserved . The evident demise of the Ediacaran fauna has resulted in two alternative hypotheses that are not entirely exclusive . One appeals to a change in taph­ onomic conditions, in particular the rise of Cam­ brian predators and scavengers that militated against soft part preservation . It is, however, of considerable significance that a distinct gap separ­ ates the disappearance of the Ediacaran fauna from the debut of Cambrian assemblages, an interval that contains facies that otherwise would appear suitable for preservation (Narbonne & Hofmann 1987) . If indeed a substantial fraction of the Ediacaran fauna became extinct over a geologically brief period, then it may be that the subsequent Cambrian diversification was largely a response to the ecological opportunities presented . The evi­ dence for such an end-Ediacaran mass extinction (Section 2 . 13 . 1) at present is very tenuous . It is necessary to emphasize, however, that as yet no data point to any extra-terrestrial mechanism. If comparisons were to be drawn with other mass extinctions, then there are possible similarities with the end-Permian event (Section 2. 13.4) in which the formation of a super-continent and possibly devel­ opment of brackish oceans because of massive evaporite deposition are invoked as significant factors .

34

1 Major Events in the History of Life

Cambrian biotas

Whether or not there was an end-Ediacaran mass extinction, the ensuing diversifications of the Cambrian were a spectacular evolutionary event (Brasier 1979; Conway Morris 1987) . Most obvious is the appearance of abundant skeletal parts (Section 1 .4) composed of calcium carbonate, calcium phos­ phate or silica, which together provide for the first time in the history of Earth an adequate fossil record. Given that the bulk of the fossil record consists of shelly fossils, it is not surprising that the many ex­ planations offered for the Cambrian diversifications have focused on the origin of hard parts. While special explanations may be called for, soft-bodied organisms may have outnumbered greatly those with skeletons in the original Cambrian communi­ ties and the history of diversification of trace fossils during this interval is also an important component in documenting these adaptive radiations. Although the rise of the skeletal faunas is clear in outline, detailed resolution is hampered by uncertainties regarding inter-continental correlations, such that the exact sequence of events is still uncertain. Present evidence, however, suggests that (apart from Cloudina) the earliest skeletal fossils included anabaritids (elongated tubes with a highly charac­ teristic trifoliate cross-section) and the teeth of protoconodonts, a group probably related to the modem chaetognaths (arrow-worms). Shortly after­ wards they are joined by more shelly fossils, in­ cluding a distinctive monoplacophoran known as Purella, the gastropod Aldanella, and primitive hyo­ liths. The succeeding horizons record an abundance of additional shelly fossils (Bengtson 1977), many of enigmatic affinities (see also Section 5.2 .5) but also including additional monoplacophorans, the first gastropods, hyoliths, brachiopods, sponges, and, somewhat later, echinoderms. The majority of these fossils are relatively small (c. 1 - 2 mm), and are either composed of phosphate or are replaced sec­ ondarily by this compound. These small shelly fossils (see also Section 1 .4) are the subject of active study, with special interest in the more enigmatic taxa (Bengtson 1977) . Although for many species biological relation­ ships are entirely speculative, in others a natural classification is beginning to emerge. Three import­ ant groups include the tommotiids, which possessed a primary phosphatic skeleton, the coelosclerito­ phorans which comprise halkieriids, siphogo­ nuchitids, and chancelloriids, and the cambroclaves,

the last two having calcareous skeletons. In each group the skeleton is composite, being composed of a series of sclerites that disarticulated on death. This extraordinary array of small shelly fossils per­ sists during the early stages of the Cambrian, es­ pecially the Tommotian and Atdabanian, with some lingering into the Middle and even Upper Cam­ brian. It is noteworthy that the trilobites, which dominate the majority of Cambrian shelly faunas, are absent from the earliest assemblages. However, their appearance in different sections was probably not synchronous, and their debut was probably due to mineralization on pre-existing forms with only a chitinous skeleton, rather than an evolutionary event per se. The rise of these skeletal faunas has been inter­ preted in both ecological terms, especially the rise of predators conferring the need for protective structure, and in terms of changes in the physico­ chemical environment (Conway Morris 1987; see also Section 1 .4) . The evidence that many groups possessed either tightly interlocking sclerites that probably formed a coat over the exterior, or valves that enclosed or allowed the retraction of the soft parts, certainly supports a response to predation. In some specimens, especially tubicolous taxa, small boreholes occur. They probably represent predatory activity, but the nature of the attacker is speculative. It is also likely that the protoconodonts formed part of a predatory feeding apparatus, but in general it is necessary to infer that many of the early Cambrian predators were more or less entirely soft-bodied. Examples of Lagerstatten that might reveal the nature of such soft-bodied organisms are not known until the Atdabanian, and of these the Burgess Shale-like Cheng-jiang fauna in Yunnan Province, South China is by far the most important. This fauna has not yet received detailed analysis, and much of our information on the role of soft-bodied organisms in the initial Cambrian diversifications must continue to rely on evidence from trace fossils (Crimes 1987) . A general diversification that paral­ lels the skeletal record is now well known. In par­ ticular, Vendian traces typically are rather small and two-dimensional. Some ichnotaxa survive into the Cambrian, but a number (e.g. Harlaniella) are re­ stricted to this interval and therefore have a bio­ stratigraphic utility. The striking increase in trace fossil diversity near the Precambrian - Cambrian boundary (Section 5. 10.2) includes vertical burrows, scratch marks that generally are attributed to arthro­ pods, and other traces that often indicate increas­ ing behavioural complexity. It is also striking that

1 .5

35

Metazoan Diversification

ichnotaxa regarded as diagnostic of either shallow­ or deeper-water where they occur later in the Phanerozoic, are found together in shallow-water environments (Crimes & Anderson 1985) . Indeed, it has been proposed that the deep oceans were not colonized until later in the Palaeozoic, and that the displacement of some trace makers into deeper water was a result of competitive pressure in the shallows. While the role of ecological changes has domi­ nated discussion on the evolution of early meta­ zoans, it now appears that substantial alterations in the extrinsic physico-chemical environment were also taking place during this time (Conway Morris 1987) . The extent to which such changes influenced or even controlled evolutionary events is far from clear, although the near synchronous nature of them is certainly suggestive . Changes in the physico-chemical environment

Extrinsic changes are registered in several ways, including: palaeocontinental distributions, sea­ level curves, stable isotope variations (especially of carbon and sulphur), preference for either aragonite or calcite precipitation, and phosphate deposition . While the extent and nature of the late Precambrian super-continent is still under debate, there is clear evidence for major rifting episodes close to the Precambrian - Cambrian boundary that heralded its break-up . While the separation of continental

blocks would have encouraged the development of endemic faunas, the formation of hot, spreading ridges would have led to displacement of seawater and hence a major transgression . While the history of this Cambrian transgression is not well known in detail, it had the dual effect of increasing the habit­ able area for shallow-water marine life and pro­ viding an increasingly complete rock record as the facies belts migrated cratonward (Brasier 1979) . There is also evidence for substantial changes in ocean chemistry close to the Precambrian ­ Cambrian boundary (Fig . 2) . For example, measure­ ments of sulphur isotopes ({'\345) from very late Rrecambrian evaporites record a massive positive shift (the Yudomski event) that reflects the intro­ duction of substantial amounts of isotopically heavy seawater into areas of evaporite formation by some sort of upwelling. The shift is so significant that it probably represents long-term storage of deep­ water brines, where bacterial fractionation of sul­ phur led to accumulation of increasingly 'heavy' water. The sites of such storage may have been narrow 'Mediterranean-like' basins formed at an early stage of continental breakup, and the up­ welling episode may also be linked to continuing evolution of the basins. It is probably no coincidence that the Yudomski event overlaps with a major episode of phosphogenesis, that is now reflected in huge economic reserves of phosphate in China and elsewhere . It has been speculated that the influx of phosphorous raised levels of productivity and

Metazoan d ivers ificat i o n (fam i l ies)

Fig. 2

Changes in ocean chemistry as registered in O BC and 0345, inferred sea-level, and diversity of metazoans and stromatolites during intervals of the Riphean, Vendian and Cambrian. (Data for stromatolites from Waiter & Heys 1985; other data sources listed in Conway Morris 1987.)

Ri h ean 1 000

950

900

850

800

750

700

650

600

550

500 ( 1 06 yrs)

1 Major Events in the History of Life

36

helped to fuel the evolutionary radiations. Infer­ ences on ocean productivity have also been drawn on the basis of changes in carbon isotopic ratios (613q, which show a series of substantial shifts. However, in some instances storage of organic mat­ 2 ter (rich in photosynthetically sequestered 1 q, such as in anoxic basins, may be invoked as an explanation and could be linked to the formation and destruction of narrow marine basins alluded to above. Although somewhat less constrained in terms of timing, there is also evidence for a shift in inorganic precipitation (e.g. ooids) of calcium car­ bonate polymorphs, from aragonite in the late Pre­ cambrian to calcite in the Cambrian. The reasons for this shift are complex, but stem from processes of plate tectonics. These include hydrothermal metamorphism at spreading ridges that lower the Mg: Ca ratio of seawater, rise of partial pressure of CO2 by volcanic exhalations, and deposition of carbonates in shallow seas versus their weathering on exposed continents. Taken together, the shift towards calcite precipitation appears to be con­ trolled in part by continental breakup, growth of spreading ridges and subduction zones, and transgression of continental margins. Just how important extrinsic factors, most of which seem to stem ultimately from the processes of plate tectonics, were in controlling evolutionary events is still uncertain. Metazoan diversification may have had its roots far back in the Riphean but, as yet, the possible influence of extrinsic factors on biological evolution in this interval is largely specu­ lative. Nevertheless, the rise of skeletons near the Precambrian-Cambrian boundary can be linked with slightly more confidence to changes in ocean chemistry, and it is interesting that similar suggest­ ions have also been made in connection with skeletal evolution during the great Permo-Trias faunal turn­ over. Some workers have even suggested that en­ vironmental factors may have led to sequential mineralization, from aragonite to high magnesium calcite to phosphate to low magnesium calcite (Brasier

1986). The complexity of the processes and

the paucity of evidence in several critical areas, however, make this a challenging area for future palaeobiological research.

References Bengtson, S . 1977. Aspects of problematic fossils in the early Palaeozoic. Acta Universitatis Upsaliensis 415, 1 - 71 . Brasier, M . D . 1979 . The Cambrian radiation event. In : M.R. House (ed . ) The origin of major invertebrate groups. System­ atics Association Special Volume 12, pp. 103- 159. Academic Press, London. Brasier, M . D . 1986 . Precambrian-Cambrian boundary biotas and events. In: O. Walliser (ed .), Global bio-events . Lecture Notes in Earth Sciences No . 8, pp . 109 - 1 17. Springer­ Verlag, Berlin. Conway Morris, S. 1985 . The Ediacaran biota and early metazoan evolution. Geological Magazine 122, 77- 8 1 . Conway Morris, S . 1987. The search for the Precambrian­ Cambrian boundary. American Scientist 75, 156 - 1 67. Crimes, T.P. 1987. Trace fossils and correlation of late Pre­ cambrian and early Cambrian strata. Geological Magazine 124 , 97- 1 1 9 . Crimes, T.P. & Anderson, M.M. 1985 . Trace fossils from later Precambrian-early Cambrian strata and environmental implications. Journal of Paleontology 59, 310-343. Gehling, J . G . 1987. Earliest known echinoderm - a new Ediacaran fossil from the Pound Subgroup of South Australia. Alcheringa 11, 337-345 . Glaessner, M . F . 1984. The dawn of animal life. A biohistorical study. Cambridge University Press, Cambridge. Grant, S.W.F. 1990. Shell structure and distribution of Cloudina, a potential index fossil for the terminal Protero­ zoic. American Journal of Science 290A, 261 - 294. Harding, S . c . & Risk, M.J. 1986. Grain orientation and elec­ tron microprobe analyses of selected Phanerozoic trace fossil margins, with a possible Proterozoic example. Journal of Sedimentary Petrology 56, 684 - 696. Hori, H . & Osawa, S . 1987. Origin and evolution of organ­ isms as deduced from 5S ribosomal RNA sequences . Molecular Biology and Evolution 4 , 445-472. Kauffman, E . G . & Steidtmann, J.R. 1981 . Are these the oldest metazoan trace fossils? Journal of Paleontology 55, 923947. Narbonne, G . M . & Hofmann, H.J. 1987. Ediacaran biota of the Wemecke Mountains, Yukon, Canada. Palaeontology 30, 647- 676. Seilacher, A. 1984. Late Precambrian and early Cambrian Metazoa: preservational or real extinctions? In: H . D . Holland & A.F. Trendall (eds) Patterns of change i n Earth evolution, pp. 159 - 168 . Springer-Verlag, Berlin. Seilacher, A. 1989 . Vendozoa: organismic construction in the Proterozoic biosphere. Lethaia 22, 229 -239 . Sun Wei-guo, Wang Gui-xiang & Zhou Ben-he 1986. Macro­ scopic worm-like body fossils from the upper Precambrian (900- 700 Ma), Huainan district, Anhui, China and their stratigraphic and evolutionary significance . Precambrian Research 31, 377- 403. Waiter, M.R. & Heys, G . R . 1985 . Links between the rise of the Metazoa and the decline of stromatolites . Precambrian Research 29, 149 - 1 74.

1.6 Evolutionary Faunas J. J.

SE PKO SKI ,

Jr

Evolutionary faunas are sets of higher taxa (es­

Phanerozoic and the total number of classes has

pecially classes) that have similar histories of diver­

remained virtually constant since.

sification and together dominate the biota for an

The expansion of each evolutionary fauna is as­

extended interval of geological time. The expansion

sociated with the decline of the previously dominant

and decline of evolutionary faunas can be used to

fauna. The declines are much slower than the initial

describe large-scale variations in faunal dominance

diversifications, giving the faunas very asymme­

and to interpret temporal changes in global taxo­

trical histories. Such a pattern is difficult to simulate

nomic diversity in the fossil record. The concept

in 'random' models of diversification (Sepkoski

was introduced by Sepkoski

(1981),

1981)

who identified

but can be described with coupled logistic

equations of the form

three 'great evolutionary faunas' in the Phanerozoic marine record. These faunas were defined statisti­

dDJ d t

cally in a factor analysis of familial diversity within

Dj

=

rjDj (1 - L D/ Dj),

taxonomic classes, which grouped together classes

where

that attained their maximum diversities around the

is the diversity of the ith evolutionary

t, rj is its initial diversification Dj is its maximum or 'equilibrium' diversity, and LDj is the summed diversity of all faunas at time t (Sepkoski 1984; Kitchell & Carr in Valentine fauna at time

same time. The analysis permitted the histories of

rate,

the aggregate faunas to be traced from initial diver­ sification through dominance and into decline. This treatment of the faunas as units throughout their

1985) .

histories distinguishes the concept of evolutionary

fauna will diversify and replace the preceding fauna

faunas from that of 'dynasties',

only if its initial diversification rate is lower and

used by some

This equation states that an evolutionary

rj

authors for assemblages of dominant taxa during

equilibrium diversity is higher. If

specified intervals of geological time.

evolutionary fauna will expand so rapidly that the

is higher, the

preceding fauna will never appear to diversify; if

Dj

is lower, the evolutionary fauna will never be able

Marine evolutionary faunas

to expand and replace the preceding one. Thus, the

Characteristics .

The three evolutionary faunas iden­

bility in the sequential diversification of evolution­

tified in the marine fossil record are the Cambrian

ary faunas, although it does not specify their timing

Fauna, important during the Cambrian Period, the

or relative differences in maximum diversity.

coupled logistic equation suggests a certain inevita­

Palaeozoic Fauna, dominant from Ordovician to

Classes within evolutionary faunas tend to have

Permian, and the Modern, or Mesozoic-Cenozoic

similar mean rates of taxonomic turnover. Classes

Fauna, dominant in the post-Palaeozoic (Fig. lA).

in the Cambrian Fauna tended to have high turnover

The classes in each fauna share a number of charac­

rates, those in the Palaeozoic Fauna intermediate

teristics, or central tendencies, suggesting that they

rates, and those in the Modern Fauna comparatively

are not randomly assembled groups of taxa. The

low rates (with some exceptions in all cases). These

most striking characteristic is that the classes tend

differences are reflected in the responses of the

to diversify together, each successive fauna dis­

faunas to mass extinctions (Sepkoski

playing a slower rate of diversification but higher

Cambrian Fauna suffered large proportional re­

1984) :

the

level of maximum diversity than those preceding

ductions in diversity relative to the Palaeozoic fauna

it. These properties lead to a sequential expansion

during mass extinctions in the Ashgillian and

of evolutionary faunas and a resultant step-like

Frasnian, and the Palaeozoic Fauna suffered more

pattern of increase in global marine diversity (with

than the Modern at all major mass extinctions of the

the step between the Palaeozoic and Modern faunas

Phanerozoic. This differential reaction seems to

disrupted by the massive Late Permian extinction

have led to the great change in faunal dominance

event - Section 2 . 13.4) . This pattern is present even

associated with the Late Permian mass extinction

though most marine classes originated early in the

(Section

37

2 . 13.4) .

1 Major Events in the History of Life

38 900

.'!::

E � '0 '"

E

600

�

Q) .D

:::J Z

300

1 Diversity curves . A, Marine animal families. B, Terrestrial vascular plant species. C, Terrestrial tetrapod families . Each curve is divided into fields that illustrate the diversities of the constituent evolutionary faunas and floras . A, After Sepkoski (1984) ; Cm Cambrian evolutionary fauna, pz Palaeozoic fauna, Md Modern fauna; stippled field represents known diversity of families with rarely preserved members that lack heavily mineralized skeletons . B, After Niklas et al. (1983); numbered fields as in text. C, After Benton (1985); numbered fields as in text. Fig

600

400

200

600

·E � '0 '"

Q)

'"

u

Q)

'0

Q) Cl.

'"

0

400

E 200

200

=

=

�

�

Q) .D

Q) .D

:::J z

:::J Z

E

0

100

0 400

200

0

=

D

400

Geological time (106 yrs)

Evolutionary faunas also seem to have differing ecological characteristics . The Cambrian Fauna tended to be assembled into broadly intergrading communities that were dominated by generalized deposit feeders and grazers and had low epifaunal and infaunal tiering (Bottjer & Ausich 1986; see also Section 1 . 7. 1 ) . Communities of the Palaeozoic Fauna were dominated by epifaunal suspension feeders with complex tiering; many other ecological guilds were also represented so that the fauna as a whole seems to have occupied more 'ecospace' than the Cambrian Fauna (Bambach in Tevesz & McCall 1983) . Finally, the Modern Fauna is represented by yet more guilds and is characterized by large numbers of durophagous predators (Vermeij 1987) and mo­ bile deep infauna (Thayer in Tevesz & McCall 1983); epifaunal tiering is reduced in most communities . Sepkoski and Miller in Valentine (1985) demon-

200

0

strated that evolutionary faunas tended to form coherent assemblages within shelf environments throughout the Palaeozoic Era . Members of the Cambrian Fauna were spread across the entire shelf early in the Palaeozoic Era but became progressively restricted to deeper-water environments during the Ordovician as members of the Palaeozoic Fauna expanded across the middle and finally outer shelf. At the same time, early members of the Modern Fauna came to dominate inner shelf environments and later, deeper, low-oxygen environments . The Late Permian mass extinction eliminated dominance of the Palaeozoic Fauna from middle and outer shelf environments and led to expansion of the Modern Fauna across the entire shelf. It must be emphasized that none of these evo­ lutionary and ecological differences between the faunas is absolute . In a sense, the faunas are 'fuzzy

39

1 . 6 Evolutionary Faunas bounded sets' with their characteristics overlapping

2.

and some members of each fauna mimicking mem­

bites along with inarticulate brachiopods, mono­

bers of others. The characteristics thus represent

placophorans, hyoliths, and eocrinoids; most of the

nodes on a continuum. Major unsolved problems

problematical taxa of the so-called 'small shelly

are why such nodes should exist and why they

faunas' of the Tommotian are also included. Various

The Cambrian Fauna was dominated b y trilo­

of these classes are paraphyletic, with descendent

seem to change so little through the Phanerozoic.

monophyletic taxa belonging to other evolutionary

Composition and history.

The individual histories of

faunas; however, in most cases the paraphyletic

the marine evolutionary faunas are illustrated in Fig.

classes either declined long before their descendent

CAM B R I A N F A U N A

I n a rt i c u lata T r i l o b ita

Hyo lit h a

�

M o n o p lacop h o ra

' ,.

200E �

Eocr i n oidea

(J) �

������--���T� O

� Z

PA LAEOZO I C FAU NA

A rt i c u l ata A n t h ozoa

C e p h a l opoda

S t e n o l a e m ata

Ste l l e r o i d a

400 200 '0

O s t racoda

C ri no idea

M O DE R N FA U NA

�� Repti l i a

Osteic h t hyes

Biva lvia

600 Malacostraca

C h o n d ric h thyes

E 400 � '0

G a s t ropoda

2 Histories of the three great evolutionary faunas of the marine fossil record as represented by their familial diversities through the Phanerozoic. Representatives of the important classes in each fauna are illustrated above the diversity curves. (After Sepkoski 1984.) Fig

o

200 Gym n o l ae mata

600

400 G eo l o g i c a l t i m e

E

.D

D e m o s p o n g i a R h izopodea Ech i n o i d e a

200 (106 yrs)

o

i

40

1 Major Events in the History of Life

taxa diversified (e .g. the Monoplacophora) or con­ tained monophyletic subtaxa that diversified in parallel with the rest of the evolutionary fauna (e .g. the Inarticulata) . The Cambrian Fauna diversified very rapidly from the latest Vendian into the Early Cambrian and was the principal constituent of the 'evolutionary explosion' across the Precambrian ­ Cambrian Boundary (see also Section 1 .5) . Its maxi­ mum diversity was attained in the late Middle and early Late Cambrian . Beginning in the latest Cambrian, the fauna began a long, gradual decline, accentuated by the Ashgillian and Frasnian mass extinctions (Sections 2 . 13.2, 2 . 13.3) . The Palaeozoic Fauna initiated its expansion as the Cambrian Fauna began to decline; this combi­ nation resulted in nearly stable global diversity throughout the Late Cambrian. The Palaeozoic Fauna was dominated by articulate brachiopods with important contributions from crinoids, corals, ostracodes, cephalopods, and stenolaemate bryo­ zoans . These groups were major components of the Ordovician radiations, which tripled global taxo­ nomic diversity over a 50 million year interval . The Palaeozoic Fauna attained its maximum diver­ sity from the Late Ordovician to Devonian and then began a long decline . During the Carboniferous and Permian, this decline was matched by a slow ex­ pansion of the Modem Fauna so that again global diversity remained nearly constant . The Palaeozoic Fauna was severely reduced by the Late Permian mass extinction (Section 2. 13.4) but in the Mesozoic underwent two radiations : one in the Triassic, ter­ minated by the Norian mass extinction (2 . 13 .5), and a second, slower expansion in the Jurassic . The Jurassic expansion was reversed in the Cretaceous when global diversity exceeded Palaeozoic levels, and the remnants of the Palaeozoic fauna again went into decline . The Modem Fauna is dominated by gastropod and bivalve molluscs, osteichthyan and chond­ richthyan fishes, gymnolaemate bryozoans, mala­ costracans, and echinoids . Most of these classes appeared during the Cambrian and Ordovician Periods but diversified only slowly through the Palaeozoic Era . They suffered minor extinction rela­ tive to the Palaeozoic fauna during the Late Perrnian and became the dominant fauna in the Triassic. Through the Mesozoic and Cenozoic, the Modem Fauna continued the rather slow and steady diver­ sification initiated earlier, producing the long post­ Palaeozoic increase in global taxonomic diversity. Throughout their histories, the three 'great' evo­ lutionary faunas experienced considerable internal

turnover, with continuous change in ordinal and lower-level taxonomic composition . This was par­ ticularly true of the Cambrian Fauna, which under­ went very rapid changes during its initial radiation. It may prove useful to subdivide this fauna and define two more evolutionary faunas : an Ediacaran Fauna, encompassing the distinctive soft-bodied animal fossils of the Vendi an (Sections 1 . 3, 1 .5), and a Tommotian Fauna, comprising the mostly prob­ lematical skeletal taxa of the earliest Cambrian (Sec­ tions 1 .4, 1 .5, 5.2 .5) . These possible faunas seem to fit into the general progression of evolutionary rates and diversity levels observed for the three great evolutionary faunas. The Ediacaran and especially Tommotian taxa appear to have had higher diversi­ fication rates and more rapid evolutionary turnover than the remainder of the Cambrian Fauna, and seem to show successive increases in diversity lead­ ing into the Cambrian Period . Further analysis of diversity patterns and faunal change in the Vendian and Early Cambrian are needed to assess whether such additional evolutionary faunas are useful for describing the early metazoan radiation .

Terrestrial biotas The concept of evolutionary faunas has proved use­ ful for organizing faunal turnover and diversity change in the marine record and has been extended with varying success to other evolutionary systems, specifically terrestrial vascular plants and tetrapod vertebrates . Niklas et al. (1983) identified four major plant groups, which can be termed evolutionary floras, in species-level data on tracheophyte diversity (Fig. lE). These are: (1) an initial Silurian-Devonian flora of early vascular plants that radiated and then disappeared during the Devonian; (2) a pteridophyte­ dominated flora, including ferns, lycopods, sphenop­ sids, and progymnosperms, that diversified in the Late Devonian and Early Carboniferous and domi­ nated plant communities to the end of the Palaeozoic Era; (3) a gymnosperm-dominated flora of seed plants that appeared in the Late Devonian and rose to domi­ nance in the Mesozoic; and (4) an angiosperm flora that originated in the Early Cretaceous and rapidly radiated to dominance thereafter, replacing the pre­ ceding gymnosperm flora . As in the marine system, each of these floras (excepting the angiosperms) originated early in the history of vascular plants and radiated sequentially to produce step-like increases in global tracheophyte diversity. Three 'assemblages' of terrestrial tetrapod families

1 . 7 Diversification of Marine Habitats have been identified by Benton (1985) in the ver­ tebrate fossil record (Fig . Iq. These comprise : (1) the labyrinthodonts, anaspids, and synapsids, which appeared during the Middle Palaeozoic and completely dominated the terrestrial vertebrate record to the end of the Palaeozoic; (2) the early diapsids, dinosaurs, and pterosaurs, which arose in the Triassic, attained maximum diversity in the Late Jurassic and Cretaceous, and disappeared at the terminal Cretaceous mass extinction (Section 2 . 1 3 . 7); and (3) the lissamphibians, turtles, croco­ diles, lizards, birds, and mammals, which originated in the Triassic and Jurassic, expanded through the Cretaceous, and then diversified to very high levels in the Cenozoic. Although these assemblages have some similarities to marine evolutionary faunas, there are some important differences : the assem­ blages do not all appear early in the history of tetrapods and their sequential diversifications are not all associated with step-like increases in global diversity . It remains to be seen whether such pat­ terns could be identified if more terrestrial taxa (e . g . the arthropods) were included and analyses per­ formed at lower taxonomic levels . If so, evolutionary

41

faunas and floras would appear to be a general property of the development of Phanerozoic biotas .

References Benton, M.J. 1985. Patterns in the diversification of Mesozoic non-marine tetrapods and problems in historical diver­ sity analysis . Special Papers in Palaeontology 33, 185 - 202 . Bottjer, Dj. & Ausich, W.!. 1986. Phanerozoic develop­ ment of tiering in soft substrata suspension-feeding com­ munities . Paleobiology 12, 400-420. Niklas, K.J . , Tiffney, B . H . & Knoll, A.H. 1983. Patterns of vascular land plant diversification . Nature 303, 614- 616. Sepkoski, J.J., Jr. 1981 . A factor analytic description of the Phanerozoic marine fossil record . Paleobiology 7, 36-53. Sepkoski, J . J . , Jr. 1984. A kinetic model of Phanerozoic taxo­ nomic diversity. III . Post-Paleozoic families and mass ex­ tinctions. Paleobiology 10, 246-267. Tevesz, M .J . 5 . & McCall, P . L . (eds) 1983. Biotic interactions in recent and fossil benthic communities. Plenum Press, New York. Valentine, J.W. (ed . ) 1986. Phanerozoic diversity patterns: pro­ files in macroevolution . American Association for the Advancement of Science and Princeton University Press, Princeton. Vermeij, G.J. 1987. Evolution and escalation. An ecological history of life. Princeton University Press, Princeton .

1 . 7 Early Diversification of Major Marine Habitats

1 . 7. 1 Infauna and Epifauna

w. I . A U S I C H & D . J . B O T T J E R

Introduction Benthic marine habitats and the organisms that populate them represent an intricate and diverse ensemble . Much of the initial development and diversification of metazoans was for life in this realm. Marine benthos have invaded most types of substratum at depths ranging from the supertidal to abyssal . This array of habitats, with concomitant physical and chemical limiting factors, has probably been relatively constant through most of the Phan-

erozoic . Similarly the general trophic strategies for exploitation of marine benthic habitats has been constant. Both infaunal and epifaunal organisms developed, including suspension feeders, deposit feeders, predators, scavengers, grazers, and others . However, through eustatic changes in sea-level and plate motion in the lithosphere, the habitat location has been constantly changing. The great diversity in this benthic system is con­ tributed by organisms . At any one time organisms

42

1 Major Events in the History of Life

differentially adapt to a plethora of physical, chemi­ cal and biological limiting factors . The development of simple to complex ecological structuring within habitats is variable; and, of course, through evo­ lution and extinction, the organisms populating benthic habitats have been continually in flux .

The benthic habitat

The infauna. In modern environments particulate organic material is abundant immediately above and below the sediment - water interface and de­ creases in quantity both up into the water column and down into the sediment (Fig. 1 ) . Both suspen­ sion feeders and deposit feeders exploit this re­ source . Infaunal deposit feeders mine particulate organics within the sediment, whereas infaunal suspension feeders typically feed from the water that is immediately above . The primary physical constraints on depth of burrowing are the position of the redox boundary, and sediment stiffness, which increase with depth . Phylogenetic constraints on the development of specialized structures (e . g . fused siphons) have also been important i n the history of the infauna . Infaunal suspension feeders are largely stationary . They all feed as active suspension feeders from water immediately above the sediment surface, and particulate food in that water moves past them horizontally . In contrast, infaunal deposit feeders are mobile, and they feed on a stationary food

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resource s cattered through the upper part of the sediment column (Bottjer & Ausich 1986) . Durophagous predation, space competition, and adaptation to conditions in the intertidal zone are considered to have been important influences in the development of infauna and in changes in infaunal tiering structure . Increased durophagous predation pressure led to greater infaunalization of the benthos and may have also promoted the devel­ opment of more complex infaunally tiered com­ munities . Different authors have argued eithe r that densities of infaunal bivalves are generally too Iow for space competition to be important, or that space competition can be important to avoid interference competition among suspension feeders which all feed from the same basic resource (Bottjer & Ausich 1986) . For infaunal deposit feeders, space compe­ tition may be much more important. The initiation of deep burrowing may have re­ sulted from adaptations to life in the intertidal zone, where regular fluctuations in the water table are driven by the tidal cycle . Organisms in the intertidal zone track these water table changes . The ability of infauna to cope with such conditions may have preadapted them to medium- and deep­ burrowing habits in the subtidal zone (Bottjer & Ausich 1986) .

The epifauna. Epifaunal suspension feeders live within the benthic hydrodynamic boundary layer, i . e . the zone of diminished current velocity caused by drag across the bottom . Current velocities are

F o o d r e s o u rc e s of water m a s s: d i ss olved & collo idal orga n i c m o l ec u l e s , s u s p e n d e d part i cles, swi m m i ng & floa t i n g orga n i s m s. Orga n i c conce n trat i o n low c o m pared to s e d i m e n t-water i nterface , b u t large volu m e s of m aterial pass a given p o i n t over t i m e. Water i m med iate ly a bove s ed i m e n t-water i n terface: enriched by re s u s p e n d e d part i c u late materi al. Sed i m e n t-water i n terface: h ig h concentrat i o n of orga n i c m ater i a l . Locat i o n of b e n t h i c e p i fa u n a & all b e n t h i c flora. Depos i t i o n of dead orga n i s m s and orga n i c detri t u s.

H i gh concentrat i o n of n u tr i e n t orga n i c m aterial i n sed i m e n t w i t h i n 5 cm o f sed i m e n t-water i n terface. All categor i e s of food except live pla n ts.

Decrea s i n g orga n i c content with depth, a res u lt of bacterial deco m p o s i t i o n. Aero b i c bacteri a d ecrease & a naero b i c i n crease with depth.

At d e p t h bacterial activity red uced (pre s e n t to at least 75 c m ) . Orga n i c m aterial refractory, Q U A N T I TY OF O RGAN I C not a food reso urce. • MATIER

Fig. 1 Location of food resources with respect to the sediment- water interface . (From Walker & Bambach 1974.)

43

1 . 7 Diversification of Marine Habitats lowest immediately above the sea floor and increase upward into the water column (Fig . 2). The thickness of the boundary layer is a function of factors such as current velocity and substratum roughness; how­ ever, velocity always decreases toward the ocean floor. Given equal concentrations of particulate organics, more food would be available to a suspen­ sion feeder where current velocities were greater, i . e . higher within the boundary layer; however, particulate organics generally increase toward the ocean floor. In this physical setting epifaunal sus­ pension feeders, which are largely stationary, must expl oit a food resource that is moving past them horizontally at specific distances above the sediment - water interface . Many constraints and processes are likely to have been important for the development and mainten­ ance of epifaunal tiering (Bottjer & Ausich 1986) . Phylogenetic constraints on structural materials and modes of growth, as well as the biomechanical properties of structural materials, strongly influence the height to which organisms can reach above the sea floor . The mode of growth and whether organ­ isms are clonal or aclonal are important constraints controlling an organism's � xploitation of food re­ sources within the benthi c boundary layer . Only clonal organisms (e .g. bryozoans, corals), and aclonal organisms that grow by addition of new parts (e . g . stalked echinoderms) have been able to develop medium- to high-tiered forms (Bottjer & Ausich 1986; see also Sections 4 . 5, 4. 16) . The mode of suspension feeding also appears to be correlated with utilization of epifaunal resources . Three basic suspension feeding modes have been defined : passive, facultatively active, and active . Passive suspension feeders rely completely on ambient currents for food supply, whereas facultat­ ively active suspension feeders rely to a large extent on ambient currents but also pump a weak current of water into the filtration apparatus . Active sus­ pension feeders rely on pumping water . Ecological studies and documentation of the historical record (Bottjer & Ausich 1986) show that passive and facul­ tatively active suspension feeders alone develop morphologies to become high level primary tier feeders in the epifauna . In contrast, active suspen­ sion feeders are dominant low in the boundary layer . Competition, in conjunction with other processes and constraints, has surely played a key role in the development of ecological structure in epifaunal benthos . Space, a place from which to feed, and food competition have been important for suspen-

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I

sion feeding benthos on soft substrata (Bottjer & Ausich 1986) .

Tiering. Spatial separation and structuring is a com­ mon biological method of resource partitioning within communities . Vertical community structure has been documented for epifaunal and infaunal suspension feeding communities (Bottjer & Ausich 1986) and infaunal deposit feeding communities (Levinton & Bambach 1975) . Bottjer & Ausich (1986) called this spatial arrangement of organisms tiering . They developed a history of tiering complexity through the Phanerozoic for suspension feeding palaeocommunities in soft substrata, deposited in subtidal shelf and epicontinental sea settings at depths greater than several metres below fair­ weather wave base (Fig . 3) . A comprehensive Phanerozoic history of tiering for deposit feeding palaeocommunities in these environments has yet to be compiled . Evidence for such a history, which must come primarily from studies on various fea­ tures of bioturbation (cross-cutting relationships of trace fossils, burrow depths, extent of reworking) is currently being developed (e .g. Crimes & Anderson 1985; Wetzel & Aigner 1986; Droser & Bottjer 1988) . The suspension feeder tiering history (Fig . 3) displays the maximum heights and complexity of tiering in a characteristic benthic palaeocommunity at various times . Physically dominated settings are unlikely to support a biota with this maximum development of tiering complexity . The tiering his­ tory is of primary tier feeders (Bottjer & Ausich 1987), which are organisms whose body or burrow intersects the sea floor . Although detailed tiering

1 Major Events in the History of Life

44 7ii � .J. Q; c Q;

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-0 u Q; u ..c '" �'t:

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g .� Q; u c

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•

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u

'0 N 0

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Fig. 3 Tiering in soft-substrata suspension-feeding communities through the Phanerozoic. The heaviest lines represent the maximum level of tiering above or below the substratum at any time. Other lines represent levels of tier subdivision. Solid lines represent data, and dotted lines are inferred levels. (From Bottjer & Ausich 1986 .)

histories have not been compiled for other major environmental settings, such as reefs or hard­ grounds, they should reflect the relative changes in suspension feeder tiering.

Faunal histories and ecological structure Faunal diversifications and the history of benthic faunal ecological structure can be understood best in the context of temporally distinct faunas, which include the following : Vendian Fauna, Tommotian Fauna, Cambrian Fauna, Palaeozoic Fauna, and Modern Fauna . Sepkoski (1984; Section 1 .6) defined the Cambrian Fauna, Palaeozoic Fauna, and Modern Fauna based on familial diversities .

Vendian Fauna. Fossils o f the first benthic 'metazoans' are known from the Vendian (c. 620 570 Ma) . This fauna (Sections 1 .3, 1 .5) was initially best described from the Ediacaran Hills in South Australia, but is now recognized world-wide (Glaessner 1984) . Glaessner (1984, page 52) recog­ nized 31 named species from the vicinity of Ediacara and assigned these fossils principally to modern metazoan groups, including Hydrozoa, Scyphozoa, Conulata, colonial Cnidaria, Polychaeta, and Arthro­ poda . Seilacher (1984) offered a sharply contrasting interpretation for the Vendian Fauna . He argued that many fossils interpreted as medusoids are actually trace fossils and that the non-medusoid fossils represent a clade distinct from all extant metazoans . Clearly the zoological affinities and autecol ogy

of Vendia n taxa must be understood before com­ munity ecological structure can be reconstructed. However, whatever the trophic habit of members of the Vendian Fauna, it is apparent that Vendi an communities displayed some ecological structure . Charniodiscus and Glaessnerina sp ecies apparently attained variable heights above the sea floor . Maxi­ mum preserved heights of individuals include the following : G . grandis, 16 cm; C. longus, 25 cm; C. arboreous, 60 cm . Other organisms lived directly on the bottom . It is possible that this height distinction among members of the Vendi an Fauna may rep­ resent an ecological structuring analogous to epi­ faunal tiering. The widely distributed Vendian Fauna apparently suffered major extinction (if not total extinction; Seilacher 1984) at the end of the Proterozoic (Section 2 . 1 3 . 1) . The Phanerozoic record of benthic faunas has always been significantly different from that present during the Vendian . Trace fossils from the Vendian are Palaeozoic in affinity and indicate that a worm-like fauna of shallow-burrowing deposit feeders existed during this time (Glaessner 1984) . Vertical dwelling bur­ rows are generally lacking, indicating that infaunal suspension feeders were rare or had not yet devel­ oped. Thus, at most a shallow infaunal tier of deposit feeders existed, up to several centimetres below the sediment- water interface, in soft sub­ strata Vendian environments .

Tommotian Fauna. The first major occurrence of fos­ silized metazoan hard parts was during the Tommotian at the base of the Cambrian (c. 570 Ma) . The Tommotian Fauna preceded the first occurrence of trilobites, which was approximately at the base of the Atdabanian (c. 560 Ma) (Conway Morris 1987) . This fauna (Sections 1 .4, 1 .5) is recorded by a variety of very small, principally phosphatic skel­ etons . Characteristic taxa include small conical shells such as Protohertzina and Anabarites, inarticulate brachiopods, the sclerites of Lapworthella, archaeo­ cyathids, and trace fossils (e . g . McMenamin 1987) . Like the Vendian Fauna, the Tommotian Fauna has recently been documented to occur worldwide . More autecological study on elements of the Tommotian Fauna is necessary before the palaeo­ ecological structure of these early Phanerozoic communities can be fully understood . Problems include ( 1 ) which of the component taxa are skeletal remains of single organisms and which are sclerites of some larger creature (for example Halkieria; Conway Morris 1987) ; and (2 ) the autecology and

1.7

45

Diversification of Marine Habitats

functional morphology of Tommotian organisms

+5 cm, and +5 to + 10 ern (see Fig. 4) . The +5 to + 10

that have no clear living counterpart.

cm Cambrian tier included eocrinoids, edrioaster­

Regardless

of

shortcomings

in

the

detailed

oids, crinoids, archaeocyathids, and sponges (Figs

understanding of the Tommotian Fauna, it is clear

4, 5) .

that it represents the initial establishment of the

among others, a variety of echinoderms, sponges,

basic benthic ecological structure, albeit simple and

archaeocyathids, and inarticulate brachiopods.

composed of small organisms, that would character­ ize

the

remainder

Tommotian forms,

Fauna

simple

of

the

Phanerozoic.

includes

sessile

suspension

and

feeders

The

mobile

such

as

The

0

to

+5

cm suspension feeders included,

Infaunal suspension feeders were also close to the sediment-water interface during the Cambrian. Only the

-6

cm tier was occupied in environments

&

below fairweather wave base (Bottjer

1986) .

as archaeocyathids and inarticulate brachiopods,

Cambrian inner and middle shelf carbonate deposits

and predators such as

Protohertzina

(McMenamin

1987) .

Droser

(1988)

Bottier

6

cm. If these results are typical for

such Cambrian environments, they indicate the

0

typically smaller than one centimetre. Epifaunal

continued presence of the

suspension feeders were confined to the lowest

deposit

levels within the benthic boundary layer and were

Cambrian. In contrast, deeper

probably characteristically within the tier of Bottier

&

Ausich

(1986) .

0

to

+5

reported that in

of western U.5.A. bioturbation occurs at depths no greater than

Tommotian skeletons and skeletal elements are

&

Ausich

Sinotubulites, more complex suspension feeders such

and

suspension

to

-6

cm tier for both

feeders

through

SkolitllOs,

the

possibly

cm

made by deposit feeders, is abundant in Cambrian

Trace fossils associ­

strata deposited in nearshore settings above fair­

ated with Tommotian faunas indicate that the initial appearance of vertical burrows

4-5

curred during this time (McMenamin

weather wave base, forming the typical pipe-rock.

cm deep oc­

1987)

in near­

Palaeozoic Fauna.

The Palaeozoic Fauna (Sepkoski

shore settings above fairweather wave base. In

1984;

general, though, trace fossils formed in soft substrata

from the Ordovician to the Permian and was

Section

1 . 6)

characterized benthic habitats

settings below normal wave base appear to pen­

dominated

etrate depths no greater than several centimetres in

anthozoans, ostracodes, cephalopods, stenolaemate

the substrate (e.g. Crimes the

0

to

-6

&

Anderson

cm tier of Bottier

&

Ausich

Whether driven by ecological pro­

cesses, general laws of size increase, or intrinsic diversification after approximately the

Tommotian

Fauna

was

10

million years,

replaced

by

the

Cambrian Fauna. The Cambrian Fauna represents a diversification of metazoans and an increase in body size of benthos, both of which resulted in more complex benthic communities. From analysis of familial diversities, dominant faunal elements in the Cambrian Fauna include trilobites, inarticulate brachiopods,

hyolithids,

monoplacophoran mol­

luscs, eocrinoid echinoderms, and archaeocyathids. The Cambrian Fauna dominated the benthic habitat for approximately

55

million years.

Typical preservation of a Cambrian benthic com­ munity reveals a simple tiering structure; a relatively simple structure is also evident in the Burgess Shale fauna despite preservation of the soft-bodied faunal component (Section

3.1 1 .2) .

Tiering levels for both

epifaunal and infaunal suspension feeders remained quite low (Bottier

&

Ausich

1986) .

articulate

brachiopods,

crinoids,

1985); thus (1986) was

present for both suspension and deposit feeders.

Cambrian Fauna.

by

Two tier levels

are defined for epifaunal suspension feeders:

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Mesozoic Cenozo i c

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feeders on soft substrata from non-reef, shallow subtidal shelf, and epicontinental sea settings. Vertical distribution within each tier is arbitrary and only implies occupation in a tier for the duration indicated. (From Bottjer

&

Ausich 1986.)

1

46

Major Events in the History of Life

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bryozoans, stelleroids, and graptolites . Much of the Ordovician radiation was among benthic epifaunal suspension feeders . During the Ordovician and through the Early Silurian the maximum level of epifaunal tiering and tiering complexity steadily increased from the low, simple tiering of the Cambrian . In the Middle Ordovician characteristic epifaunal tier subdivisions were 0 to +5, +5 to + 10, and + 10 to +50 cm . However, by the Middle Silurian, the maximum characteristic tier level was

Ho l o t h u ro i d e a

Fig. 5 Tiering history of Phanerozoic suspension-feeding echinoderms (details as in legend to Fig. 4) . (From Bottjer & Ausich 1986 . )

one metre, and tier subdivisions were as follows : 0 to +5, +5 to +20, +20 to +50, and +50 to + 100 cm . A characteristic Middle Silurian epifaunal commu­ nity with maximum tiering development may have contained the following: 0 to +5 cm tier - brach­ iopods, bryozoans, sponges, corals, graptolites, a few bivalves, and many echinoderms; +5 to +20 cm tier - bryozoans, sponges, corals, graptolites, and many stalked echinoderms; +20 to +50 cm tier crinoids, diploporiti ds, and perhaps blastoids; +50

1 . 7 Diversification of Marine Habitats

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Mesozo i c C e n ozo i c

Fig. 6 Tiering history o f Phanerozoic suspension-feeding bivalves (details as in legend to Fig . 4; Actinodontoida Modiomorphoida) . (From Bottjer & Ausich 1986 . ) =

to + 100 cm tier - crinoids (see Figs 3 - 6) (Bottjer & Ausich 1986) . By the Middle Silurian tiering complexity stabil­ ized and remained relatively constant until the ter­ minal Palaeozoic extinctions . Occupation of tiers by major groups was also relatively constant until the end of the Permian . Notable exceptions were the expansion of fenestrate bryozoans during the Devonian, extinction of benthic graptolites in the Carboniferous (Fig. 4), and the gradual elimination of suspension-feeding echinoderms, except for crinoids and blastoids (Fig . 5) . Exploitation of higher tier positions is a function of growth to a larger size among individuals . How­ ever, larger size alone is not sufficient to explain the high degree of tiering complexity that characterized the epifauna of the Palaeozoic Fauna . Numerous processes were responsible for the development of

47

the highly structured epifaunal communities . As explained above, these include phylogenetic con­ straints, modes of growth, intrinsic differences be­ tween clonal and aclonal organisms, adaptation of various types of suspension feeders to life in the benthic boundary layer, and competition for food and space from which to feed (Bottjer & Ausich 1986) . At the close of the Palaeozoic, tiering com­ plexity and heights must have been drastically reduced due to mass extinction (Section 2 . 13.4) . This presumption i s based on the observed faunal reductions, although a precise morphological record of this tiering decline has not been documented . Infaunal tiering complexity of suspension feeders developed more slowly than for epifauna . During the Cambrian - 6 cm was the characteristic maxi­ mum depth, and this increased to - 12 cm by at least the Early Ordovician . Consequently infaunal tier subdivisions were 0 to -6 cm and -6 to - 12 cm by the Early Ordovician, and this structure persisted until the Lower Carboniferous . Bivalves and brachiopods were typical inhabitants of the 0 to - 6 cm tier in the Ordovician, and trace fossil evidence forms the basis for indicating the presence of the -6 to - 12 cm tier at this time (Bottjer & Ausich 1986) . Bivalves began to occupy the -6 and - 12 cm tier at the beginning of the Devonian, which coin­ cides with increased levels of durophagous pre­ dation . Increased predation pressures also may have been responsible for the development of a - 12 to - 100 cm tier that began during the Lower Car­ boniferous . Both bivalves and trace fossils record the development of deep tier feeders in the Late Palaeozoic. A detailed tiering history of post-Cambrian Palaeozoic deposit feeders is not available, therefore details of the early radiation are not known . By at least the Silurian, infaunal deposit feeding bivalves had apparently developed a tiering structure through at least the 0 to -6 cm level (Levinton & Bambach 1975) . The tiering structure of Silurian deposit feeding bivalves was comparable to similar living bivalve communities (Levin ton & Bambach 1975) . If Thalassinoides in western U . S . A . Ordovician carbonate shelf deposits was made by deposit feeders, and if it can be considered to be character­ istic for this time, then deposit feeder tiering in environments below fairweather wave base may have reached depths of - 1 m early in the develop­ ment of the Palaeozoic fauna (Bottjer and Ausich 1986) . Whereas mass extinction at the close of the Palaeozoic (Section 2. 13 .4) greatly affected epifaunal

48

1

Major Events in the History of Life

organisms and the tiering structure of epifaunal suspension feeders, infaunal suspension feeders were relatively unaffected. No change in tiering structure is apparent in the record of infaunal sus­ pension feeders between the Permian and Triassic .

Modern Fauna. The Modern Fauna, characteristic of the Mesozoic and Cenozoic, has been dominated by the following benthos : bivalves, gastropods, gym­ nolaemates, malacostracans, demosponges, rhizo­ pods, and echinoids (Sepkoski 1984; Section 1 . 6) . Immediately following the terminal Palaeozoic extinction, epifaunal suspension feeder tier levels were significantly reduced, but infaunal suspension feeder tiers were not . However, by the Middle Triassic, tier heights and complexity were restored to Middle Palaeozoic levels (see Fig . 3) . Again, crin­ oids with 100 cm stems were present in shallow­ water settings . Probably the same suite of processes and constraints that was responsible for the devel­ opment of epifaunal tiering in the Palaeozoic was involved in its re-establishment during the early Mesozoic . A typical Jurassic suspension feeding community may have been composed of the fol­ lowing epifaunal organisms : 0 to +5 cm tier brachiopods, bryozoans, bivalves, sponges, corals and crinoids; +5 to + 20 cm tier - sponges, bryo­ zoans, alcyonarians, and crinoids; + 20 to + 50 cm tier - crinoids, sponges, and alcyonarians; + 50 to + 100 cm tier - crinoids . Infaunal suspension feeding organisms included a variety of bivalves (Fig . 6), gastropods, and worms and crustaceans as indicated by trace fossils (Bottjer & Ausich 1986) . Deposit feeders at this time apparently existed in a tiered structure (e .g. Wetzel & Aigner 1986), but in general the tiering structure for this trophic group has not been documented for the Mesozoic. This well developed infaunal and epifaunal sus­ pension feeder tiering complexity only lasted for approximately 100 million years . By the Cretaceous, stalked crinoids were absent from shallow-water benthic habitats, and the maximum characteristic tier height was reduced from + 100 to approxi­ mately + 50 cm. Displacement of stalked crinoids to deeper-water settings was a gradual process that may have been the result of increased levels of predation in the later Mesozoic (Bottjer & Ausich 1986) . Since the beginning of the Cretaceous, epi� faunal suspension feeders typically have not been important in soft substrata settings . Both infaunal and epifaunal suspension feeder tiering structure were relatively unaffected by the terminal Mesozoic extinction .

Post-Jurassic benthic communities in shallow­ water soft substrata settings have been dominated by infauna. This basic organization has remained relatively constant for c. 140 million years . A charac­ teristic Neogene community with maximum devel­ opment of suspension feeder epifaunal tiering would include the following: 0 to +5 cm tier bryozoans, bivalves, sponges and corals; + 5 to + 20 cm tier - bryozoans, sponges, alcyonarians; and + 20 to + 50 cm tier - sponges, alcyonarians . Charac­ teristic infaunal suspension feeding organisms would include, as for the Mesozoic, a variety of bivalves (Fig . 6), gastropods, and worms and crus­ taceans as indicated by trace fossils (Bottjer & Ausich 1986) . Deposit feeders had a tiered structure during this time in related environments (e . g . Savrda & Bottjer 1986), but, as for the Mesozoic, tiering struc­ ture for this trophic group has not been documented for the Cenozoic .

Conclusion Examination of the fossil record for trends in tiering provides a means of tracing patterns of ecological structure independently of enumerations of taxa. Only the Phanerozoic history of suspension feeding palaeocommunities from below fairweather wave base continental shelf and epicontinental sea environments is relatively well known . However, some general contrasts between infaunal and epifaunal tiering in Vendian - Recent settings can be noted . Infaunal tiering, from the beginning, has had a history of slow but steady increase in com­ plexity through attainment of greater burrowing depths and development of additional tiers . In con­ trast, if the height distinction among members of the Vendian Fauna reflects epifaunal tiering, it records the first of three periods of development of epifaunal tiering which were followed by reduction . These differences in tiering history may indicate a relatively greater resistance of the infaunal habitat to pertubations in ecological as well as evolutionary time .

References Bottjer, D.J. & Ausich, W.!. 1986 . Phanerozoic development of tiering in soft substrata suspension-feeding communi­ ties. Paleobiology 12, 400�420. Conway Morris, S . 1987. The search for the Precambrian � Cambrian boundary . American Scientist 75, 157� 167. Crimes, T.P. & Anderson, M.M. 1985 . Trace fossils from late Precambrian� early Cambrian strata of southeastern

1 . 7 Diversification of Marine Habitats Newfoundland (Canada) : temporal and environmental implications. Journal of Paleontology 59, 310�343. Droser, M . L . & Bottjer, D.J. 1988. Trends in extent and depth of bioturbation in Cambrian carbonate marine environ­ ments, western United States. Geology 16, 233�236 . Glaessner, M.F. 1984. The dawn of animal life. A biohistorical study. Cambridge University Press, Cambridge. Levinton, J.S. & Bambach, R.K. 1975 . A comparative study of Silurian and Recent deposit-feeding bivalve communities . Paleobiology 1, 97 � 124. McMenamin, M.A.5. 1987. The emergence of animals . Scientific American 256, 94� 102. Savrda, C . E . & Bottjer, D.J. 1986. Trace fossil model for reconstruction of paleo-oxygenation in bottom waters . Geology 14, 3�6. Seilacher, A . 1984. Late Precambrian and Early Cambrian metazoa : preservational or real extinctions? In : H.D. Holland & A.F. Trendall (eds) Patterns of change in earth evolution, pp. 139� 168. Springer-Verlag, Berlin. Sepkoski, J .J . , Jr. 1984. A kinetic model of Phanerozoic taxo­ nomic diversity. Ill. Post-Paleozoic families and mass extinction. Paleobiology 10, 246�267. Walker, K.R. & Bambach, R.K. 1974. Feeding by benthic invertebrates: classification and terminology for paleo­ ecological analysis. Lethaia 7, 67�68. Wetzel, A . & Aigner, T . 1986. Stratigraphic completeness : tiered trace fossils provide a measuring stick. Geology 14, 234�237.

1 . 7. 2 Plankton R . B . RICKARD S

Introduction The origin and early diversification of the Earth's plankton is largely shrouded in mystery, hypotheses leaning heavily upon a rather meagre fossil record and what seems like reasonable supposition . Con­ sider briefly the two main periods to be discussed : the Vendian and the Lower Palaeozoic . Research workers dealing with Vendian fossils have been concerned, to a large extent, with establishing that they are fossils, and much less concerned with major ecological niches . Those organisms that give least trouble with respect to identity, such as stroma­ tolites or trace fossils, are also the most obvious as regards mode of life . The more problematic creatures may yet have greater scope for the current objective, namely indicating the origin and defining the nature of early plankton . By contrast, the real problem in the Lower Palaeozoic lies in deducing the com­ position of the plankton and the relative importance

49

and functions of those components . Bulman (1964) gave a broad-based review of Lower Palaeozoic plankton: the improvements in our knowledge since then are considered below .

The Vendian The general aspect of Precambrian fossil life is not today in much dispute (Sections 1 .2, 1 . 3) . Blue­ green 'algae' (cyanobacteria or cyanophytes), the earliest proven life form, occurred at 3500 Ma and continue today . Grouped with early, reducing bac­ teria they comprise the Monera . The fossil record of the bacteria is less satisfactory, but stalked rep­ resentatives may have been involved in the cre­ ation of the banded iron formations, and it seems possible that purple and green bacteria were in­ volved with the earliest stromatolites . The question is, which prokaryotes, which Monera, could have comprised an early plankton? It is not sufficient to note that carbon isotope ratios of Precambrian black shales and dark limestones indicate an organic origin for the carbon : that merely begs the ques­ tion, as well as hiding the implication that such organic carbon must be of planktic ('algal') origin . Berry & Wilde (1983) suggested that an Archaean anoxic ocean would have had similar conditions to present day deep ocean vents, and that early carbon-fixing could have been by chemautotrophic bacteria using geothermal H2S as their primary energy source (Anoxium) . Peripheral isolates in Anoxium populations probably would have evolved to take photic energy from sunlight, because they would have been disadvantaged in the competition for reduced sulphur. Berry & Wilde (1983) also sup­ port the contention that the carbon cycle was effec­ tively stabilized by 3700 Ma (i . e . in pre-Isua time) . Their first plankton would be Anoxium isolates at the ocean surface, developing the ability to use light as an energy source, and occupying similar ecologi­ cal niches to modern purple and green bacteria . Blue-green algae share the ability with bacteria to fix their own nitrogen . They are resistant to high and low temperatures, and to dessication, and oper­ ate best in neutral to alkaline systems . Further, phycocyanin can work in very low light (it is sensi­ tive to blue light) and in consequence confers vi­ ability to depths of 1000 m and more . The modern blue-green Trichodesmium exhibits gas vacuolation, the considerable vesicular strength of which causes it to sacrifice some control of vertical mobility . In general modern blue-greens lack buoyancy control and the open ocean is considered too turbulent for

50

1 Major Events in the History of Life

their survival. The possibility that part of the devel­ opment of Trichodesmium occurs in a benthic en­ vironment may also be of adaptive significance . It is clear from this that Trichodesmium-like blue-greens in Archaean oceans would have found conditions to their liking if deductions concerning the nature of those oceans are correct; and it may partly explain the converse, that in today's oceans, despite such seeming flexibility, blue-greens are not common. (There are, however, difficulties in identifying them in plankton samples, unless epifluorescence tech­ niques are used, when blue-greens fluoresce a dis­ tinctive orange . ) Schopf ( 1976) has disputed the true fossil nature of many of the claimed Archaean microfossils, but it is widely accepted that the 3200 - 3100 Ma Archaeo­ sphaeroides (from the Onverwacht and Fig Tree Cherts) is a coccoid cyanophyte (e . g . Brasier 1979), as is Huroniospora . However, if these are truly chroococcales, then it should be noted that extant species do not fix nitrogen . By 2000 Ma (early Pro­ terozoic; Aphebian) oscillatoriacids and notocacids may well be represented . Possible Riphean micro­ fossils, which might be planktic, are almost equally contentious, but the chlorophycid Eosphaera from the Gunflint Chert was a Volvox-like green algal colony, and the p rasinophycid Tasmanites a 100 700 �m globular form with uninucleate cells. Thus the eukaryotes were probably represented in Riphean plankton. It is generally assumed that bac­ teria in general preceded cyanophytes, and that some of these could have been planktic and bacillus-like . Glaessner (1984), in his wide-ranging review of the Ediacarian fossils (Sections 1 . 3, 1 . 5), concluded that the coelomate radiation must have been pre­ Ediacarian (Varangerian), and that a change from zooplankton to benthos preceded the coelomate radiation itself. This implies the existence of zoo­ plankton in the Varangerian or earlier . Protists cer­ tainly could have been present: the Pyrrophytes begin with Arpylorus in the Silurian, but non­ tabulate forms could have occurred in profusion in the late Precambrian . Other records of Precambrian plankton include the acritarches, some of which may have been spores of multicellular algae . Acritarch occurrences in the upper Riphean to latest Precambrian have been widely documented (e . g . Vidal & Knoll 1983) . The evidence suggests that there was a gradual rise in the number of taxa from about 1400 - 900 Ma, followed by a peak and decline in the late Varangerian and Valdaian : this late Precambrian extinction event was a prelude to a

spectacular Cambrian diversity increase, to at least twice that of the lowest Vendian . In terms of Vendian palaeoecology there was a recogniz­ able division into lower diversity planktic as­ semblages in inshore environments, and higher diversity communities in offshore shelf regions or open shelf regions . With the onset o f Ediacarian time, in addition to the many benthic forms, there were undoubted medusoids. These included the chondrophorans, stiff-walled medusoids, floating at the surface and exploiting a phototrophic plankton . According to Glaessner (1984), their presence indicates that an ozone layer was then developed and that the ocean was of normal salinity and warmth . A lack of macrophagous predators may account for size increases in the zooplankton, with some medusae reaching 1 m. This model is apparently compatible with a progressive ventilation of the oceans (Berry and Wilde 1983), because Glaessner refers only to the surface layers, or to shallow shelf water bodies, which could be almost normat tropicat oxygenated marine bodies. The sequence of events in the evolution of plank­ ton in the Precambrian was probably as follows (Fig. 1 ) : 1 Chemautotrophic Anoxium a t outgassing sub­ marine geothermal vents before 3700 Ma . Such 'plankton' would have been local in distribution, above the vents? 2 Anoxium isolates began to use light energy, 3700 - 3500 Ma (and later?) . 3 Late Archaean: Archaeosphaeroides and Huronio­ spora together with bacillus-like and other bacteria, to about 2500 Ma . 4 Early Proterozoic (Aphebian) : oscillatoriacids and notocarids around 2000 Ma, with presumably more varied changes to eukaryotic microplankton . 5 Riphean: green algae well developed . 6 Varangerian: presumably development of zoo­ plankton . 7 Ediacarian : planktic medusae, often of large size; still no macrophagous predators .

The Lower Palaeozoic The Cambrian is typified by a dramatic diversity increase, mirroring that in the coeval benthos (Sections 1 . 5, 1 . 6) . The very earliest chrysophytes may have occurred at this time, an additional phyto­ plankton component, though these are typically post-Palaeozoic . Radiolarians were present in the Cambrian and equatorial in their distribution .

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52

1 Major Events in the History of Life

Foraminifera, by contrast, were almost wholly benthic throughout the Lower Palaeozoic . Larval stages (including giant larvae) of most benthic organisms were of increasing importance in the plankton, though of immeasurable proportions . One of the major components was the pelagic agnostid trilobites whose entire life cycle would have been enacted in the upper layers of the ocean . Further, there have been convincing arguments for a pelagic component in such faunas as the Burgess Shale (Section 3 . 1 1 .2) indicating the presence of a soft-bodied pelagic element . In the Cambrian there is still no direct evidence of planktic macrophagous predators, and the mix must have been composed essentially of most of the above phytoplankton groups with an increasingly diverse zooplankton . Several very major changes took place at the be­ ginning of the Ordovician . It is clear that acritarchs became an important constituent, with a major diversity peak spanning the Ordovician - Devonian periods : in some Silurian series over 2000 species have been identified in relatively small geographical regions. Radiolarians are extremely abundant in some offshore shelf graptolitic deposits (in modern tropical planktic environments they may number in excess of 80 000 individuals per m3) . The Chitinozoa, although occurring in the Cambrian, have dramatic peaks of abundance and diversity in the Ordovician and Silurian . Their occurrence in both species diversity and facies type matches that of the graptoloids, which were undoubtedly plank­ tic . Chitinozoans are presumed egg capsules of metazoans, which may not necessarily have been plankton themselves . The planktic graptoloids arose from benthic forms in the earliest Ordovician, showed considerable evolutionary development, and achieved large rhabdosomal size (approaching or exceeding 1 m in several species) . It is probable that they were the first abundant macrozooplankton, and their food was almost certainly minute phyto- and zooplank­ ton . Huge numbers are preserved in black shale formations where they are often associated with sponge spicules and what may be epiplanktic bivalves and brachiopods . There is, in addition, an increasing number of nektic elements, such as cephalopods and trilobites, yet still few large pred­ ators in the planktic environment: orthocone cepha­ lopods probably constituted the most important groups of (nektic) large predators . The graptoloids, associated closely with a vastly abundant algal phytoplankton (represented by the high carbon component of the black graptolitic shale), appear

to have dominated the Ordovician and Silurian planktic environment, but their large size may give a misleading impression of relative abundances and proportions within the plankton at the time . An understanding of the ecological diversity of grap­ toloids is still at an early stage (Rickards 1975) . They may have used gas vacuoles to control their depth within the photic zone . Other specialized features such as nemata, 'floats', vanes, webs, thecal spino­ sity, rhabdosomal stabilizers, and overall rhabdo­ somal shapes may have been designed for particular hydrodynamic roles in the plankton .

References Berry, W.B.N. & Wilde, P. 1983 . Evolutionary and geologic consequences of organic carbon fixing in the primitive anoxic ocean . Geology 11, 141 - 145 . Brasier, M . D . 1979 . The Cambrian radiation event. In: M.R. House (ed . ) The origin of major invertebrate groups. System­ atics Association Special Volume 12, pp. 103- 159 . Aca­ demic Press, London . Bulman, O.M.B. 1964. Lower Palaeozoic plankton. Quarterly Journal of the Geological Society of London 120, 455 -476 . Glaessner, M.F. 1984. The dawn of animal life. A biohistorical study. Cambridge University Press, Cambridge . Rickards, R.B. 1975 . Palaeoecology of the Graptolothina, an extinct class of the phylum Hemichordata. Biological Reviews of the Cambridge Philosophical Society 50, 397-436 . Schopf, ].W. 1976 . Are the oldest 'fossils', fossils? Origins of Life 7, 19-36. Vidal, G . & Knoll, A.H. 1983. Proterozoic plankton. Memoir of the Geological Society of America 161, 265 -277.

1 . 7. 3 Reefs C . T . SCRUTTON

Introduction Fully diversified, large scale, shelf to shelf-edge, wave-resistant organic structures like the Great Barrier Reef represent the end member of an evo­ lutionary continuum of ecosystems from small, simple, and local communities of benthic organisms . They are well developed when suitable constructors are available and poorly developed otherwise . Following important extinction events, re-establish­ ment of major reef tracts lags behind the restruc­ turing of level bottom communities, presumably

53

1 . 7 Diversification of Marine Habitats reflecting not only the availability of suitable con­ structors but the evolution of the more complex community structure associated with successful reef-building associations . Biostromes and bio­ herms are respectively sheet-like and mound-like structures dominated by skeletal organisms and either may occur in isolation or as component parts of fully differentiated reef complexes . Build-ups are any accumulations of carbonate sediment with topographic relief on the sea floor (see discussion in HeckeI 1974) .

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Phanerozoic examples, and up to the early Palaeo­ zoic, tall, narrow, erect, branched columnar mor­ phologies dominated . This is in contrast to the broader unbranched forms which subsequently dominated. Columnar stromatolite diversity in­ creased up to the Middle - Late Riphean but a sharp decline in abundance and diversity set in about 800 Ma . With the earliest claimed eukaryote being from the 1200 - 1400 Ma Beck Springs Dolomite of California, and traces of metazoans, although poorly documented and often doubtful, known from about 1000 Ma, the decline in stromatolite build-ups seems likely to reflect the rise of grazing heterotrophs . However, Copper (1974) pointed out that the first well preserved metazoans of the Ediacara fauna (Sections 1 . 3, 1 . 5) appeared not to include algal grazers, although this fauna was not recovered from carbonate facies . He timed the decline of stromato­ lites as slightly later and implicated the widespread 675 - 570 Ma Late Precambrian glaciation .

54

1 Major Events in the History of Life

The Cambrian

The Ordovician

The first metazoan reefs date from the earliest Cambrian . In clastic facies, skolithid reefs are com­ mon world-wide . They form extensive masses of agglutinated sand grains, an early equivalent of modern sabellid buildups, < 80 cm thick and hundreds of kilometres long as fringing reefs in the breaker zone cut by surge channels . Accumulated thicknesses of skolithid sands often precede the first development of archaeocyathid reefs in the Lower Cambrian, the earliest of all skeletal frame­ work reefs . Archaeocyathids, with small, usually cup-shaped, mainly solitary, porous carbonate skeletons, have been considered a distinct phylum but modern opinion tends to favour their classifi­ cation as a subgroup of the Porifera . They form mainly small patch reefs, mostly < 3 m thick and 10 - 30 m in diameter, although larger fringing or barrier reefs are claimed in the later Lower Cambrian with accumulated thicknesses < 100 m . Bioherms are dominated b y three t o four struc­ turally different genera, some rooted and func­ tioning principally as bafflers . Renalcis, Epiphyton and Girvanella are frequently associated as over­ growths and may form the bulk of the skeletal material . About 30 - 50% of the build-up is fine carbonate mud with some bioclastic debris, little pore space, and few cavities . There may be pockets or lenses of shelly material but generally fauna of the adjacent facies is rare . There is no evidence of biological destruction by borers or grazers . No obvious reef zonation is reported for archaeo­ cyathid build-ups . They are the first of a range of skeletal organisms to form patch colonizations of the sea floor with minor relief, which persist in time to form biohermal masses in the rock record . They declined at the end of the Lower Cambrian and became extinct in the early Middle Cambrian, initiating a period which, in the absence of suitable skeletal organisms, lacked significant reef growth . Algal stromatolite build-ups made a brief comeback, possibly with a decline in grazers, as gastropods are scarce in the later Cambrian (Copper 1974) . Lithistid sponges occur in some of these stromatolite masses and skeletal algae are not uncommon . Stromatolite build-ups with or without a sponge contribution persist into the early Ordovician but an explosion in diversity of grazing gastropods correlates with the effective disappearance of stromatolites as major components of build-ups on open shelves .

The early Ordovician sees a rise in small bioherms constructed of lithistid sponges, particularly Archaeoscyphia (somewhat archaeocyathid in ap­ pearance), and skeletal algae . Locally, the recep­ taculitid alga Calathium, or Pulchrilamina of dubious affinities but possibly a stromatoporoid, may be important biohermal components . Again, these mounds show no zonation and little relief, no borers but common burrowers, and increasingly diverse associated biotas including echinoderms, trilobites, brachiopods, crinoids, early bryozoans, and rich pockets of gastropods and cephalopods . Build-ups reach cumulative thicknesses of 20 m and lengths of 87 m. Larger examples may show simple suc­ cession (James 1 983), climaxing in encrustations of Pulchrilamina. In addition, the early Ordovician has the earliest examples of mud mounds dominated by the cavity structure stromatactis (variously con­ sidered as of organic or purely physical origin) and lacking any (other) sign of organic framework, < 76 m thick and 300 m across . Similar structures are recorded sporadically through the rest of the Palaeozoic, whilst stromatactis is frequently a com­ ponent of build-ups dominated by (other) metazoans . There was a great expansion in benthic marine life in the early Middle Ordovician . The stromatopo­ roids, with doubtful Cambrian representatives, the bryozoans, and the tabulate corals had all evolved and the rugose corals appeared for the first time . These groups, including the major components of the most successful Palaeozoic reef communities, diversified rapidly and non-stromatoporoid sponges declined as reef builders . However, it was almost another 100 million years before these new components realized their full potential . Initially, bryozoan reefs dominated, constructed of small encrusting, domed, massive, plus erect bifolial and cylindrical colonial morphologies trap­ ping and binding lime mud . A few small sponge reefs were bound by bryozoans and stromatopo­ roids, with blankets of shell coquinas and pelma­ tozoan debris . These mainly small, unzoned build-ups may have had as much as 1 m relief and formed accumulations up to 4 m thick, but in the later Middle Ordovician, large shelf-break carbon­ ate masses, < 250 m cumulate thickness and 60 km long, are dominated or largely constructed by bryo­ zoans (Webby 1984) . Associated faunas included crinoids, brachiopods, together with blue-green (Girvanella, Sphaerocodium) and red (Solenopora)

1 . 7 Diversification of Marine Habitats algae, some sponges and, in some of the larger build-ups, stromatactis . Tabulate coral and bryozoan build-ups coexisted briefly, with later Middle Ordovician Labyrinthitos patch reefs, but by this time the stromatoporoids were beginning to diver­ sify . From the later Ordovician until the end of the Devonian, major build-ups were dominated by stromatoporoids, with corals and skeletal algae as major contributors, whilst bryozoans and other sponges were reduced to minor roles. However, corals alone and less commonly bryozoans con­ tinued to contribute patch reefs, forming bioherms and sometimes extensive biostromes, whilst sponges sometimes dominated build-ups in deeper water. Upper Ordovician build-ups range from small patches dominated by Tetradium, fasciculate Rugosa, Receptaculita and other skeletal algae, through small algal and stromatolitic pinnacle reefs < 30 m high and 0 . 8 km in diameter, to zoned and unzoned coral - stromatoporoid build-ups and large stroma­ tactis mounds < 100 - 140 m high and 1 km in diameter. A shelf-break complex of patch reefs, individually < 15 m high and 50 m in diameter, grades from talus flanked domical stromatoporoid mounds at the margin, through communities of laminar and domical stromatoporoids, to patches of diverse corals, algae, and ramose bryozoans in the

55

shelf interior . By the late Ordovician, there is in­ creasing evidence of borers and skeleton-breaking organisms at work. The development of reef communities suffered another set-back with the late Ordovician extinc­ tions (Section 2 . 1 3 . 2) . Build-ups are few and small until mid Llandovery times . Thereafter, patch reef development becomes widespread, particularly in the later Llandovery and Wenlock, with individual examples developing < 5 m relief on the sea floor, < 60 m cumulative thickness, and 100 m or more in diameter. Succession may be well developed with pioneering faunas of syringoporids, favositids, spheroidal stromatoporoids, halysitids, or crinoid groves . In the diversification stage, stromatoporoids of various morphologies, colonial rugose corals, and tabulate corals (particularly heliolitids) may be prominent, with a rich associated fauna of brachio­ pods (often in nests), bryozoans (some cryptic), crinoids, microfauna, and stromatactis . Algae are not so prominent. Stromatoporoids, with or with­ out tabulate corals, form the domination stage . Most build-ups show little lateral differentiation internally. However, among the hundred or more patch reefs of Middle Silurian age in the Great Lakes area, the largest structures show greater com­ plexity . The 15 km2 Marine Reef of Illinois has a core largely constructed of stromatactis, with a cen-

N

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5 Fig. 2 Devonian continental reconstruction showing the distribution of organic build-ups (reefs and bioherms) and their latitudinal limits. (After Heckel & Witzke 1979 . )

56

1 Major Events in the History of Life

tral lagoonal facies, an externally fringing com­ munity of corals and stromatoporoids and a flanking apron composed largely of skeletal debris.

The Siluro - Devonian These Silurian build-ups were the forerunners of the spectacular development of reef growth in the Devonian, representing the first major peak in reef diversification and possibly the all time acme for reef ecosystems (Fig . 2) . Major reef complexes, per­ sisting over tens of millions of years, resulted in cumulative thicknesses of reef and perireefal car­ bonates < 2 km thick and stretching for hundreds of kilometres along shelves . Fringing, barrier, and shelf based atolls (faros) are represented. Reef edge, fore reef, and back reef zones are clearly differ­ entiated with detailed palaeoecological zonation comparable in complexity and in variation of con­ stituent faunas and floras to modern major reef complexes . Principal constructors of the reef mar­ gin were stromatoporoids and the blue-green algae Renalcis . Stromatactis is often present, and corals play a subsidiary role although they were more important on the reef flat and in areas where a reef rim was poorly developed or missing . Back reef facies are characterized by distinctive lithologies and assemblages, in particular by the stromatopo­ roid Amphipora. In some places, for example the Canning Basin of Western Australia, talus aprons and pinnacle reefs can be demonstrated on fore reef slopes descending to basinal facies < 180 m below contemporary sea level . Compared with Recent reefs, those of the Devonian show much less evidence of the activity of borers, grazers and scrapers; much of the break­ down of the rapidly cemented reef rock appears to have been physical .

This episode of reef building was terminated by the collapse of shallow-water ecosystems and the extinction or near extinction of the principal frame­ building organisms near the end of the Frasnian (Section 2 . 13 . 3 ) . In the Canning Basin, reef growth locally continued into the Famennian almost totally dominated by skeletal and non-skeletal algae . In the succeeding Carboniferous major build-ups are rare, although mud mounds are common, reflecting the relative paucity of suitable constructors among the skeletal organisms in the re-established level bottom communities . It was almost another 100 million years before large scale reef complexes were again developed, and then not on the scale of those of the Devonian .

References Copper, P. 1974. Structure and development of early Palaeo­ zoic reefs . Proceedings of the 2nd International Coral Reef Symposium 6, 365 - 386. Heckel, P.H. 1974. Carbonate buildups in the geologic record . In: L . F . Laporte (ed . ) Reefs in time and space, Special Publication of the Society of Economic Paleontologists and Mineralogists, No . 18 pp . 90 - 1 54. Tulsa, Oklahoma. Heckel, P.H. & Witzke, B .J. 1979 . Devonian world palaeo­ geography determined from distribution of carbonates and related lithic palaeoclimatic indicators. Special Papers in Palaeontology 23, 99- 123 . James, N . P . 1983 . Reefs . I n : P.A. Scholle, D . G . Bebout & CH. Moore (eds) Carbonate depositional environments . Memoir o f the American Association o f Petroleum Geo­ logists, No . 33, pp. 2346-2240 . WaIter, M.R. (ed. ) 1976. Stromatolites . Developments in Sedi­ mentology, No. 20. Elsevier, Amsterdam. Webby, B . D . 1984. Ordovician reefs and climate : a review. In : D . L . Bruton (ed . ) Aspects of the Ordovician System . Palaeontological Contributions from the University of Oslo, No . 8, pp. 87-98.

1 . 8 Terrestrialization

1 . 8 . 1 Soils

daily wetting and drying and to salinity variations . A s such they were preadapted t o life on land . Some silicified Precambrian forms can be compared di­ rectly to extant cyanobacteria found in subaerial settings (Campbell 1979) . In present day environ­ ments, too hostile for higher plants (such as deserts or at high altitude), primitive microbial communi­ ties are dominated by cyanobacteria, both filamen­ tous and coccoid, and chlorophytes . If such forms are capable of widely colonizing modern deserts, it would be naive to doubt their ability to colonize the ancient land surfaces . Golubic and Campbell (1979) have compared the mid-Precambrian microfossil Eosynechococcus moorei with the extant cyanobac­ terium Gloeothece coerulea, which is a sub aerial form, providing a suggestion of the earliest terres­ trial microbiota . Biogenically influenced terrestrial to supra tidal phosphates have been recorded from the Middle Cambrian of the Georgina Basin of Northern Australia (Southgate 1986) . In these examples very well preserved phosphatized microbial tubes, identical to calcified fungal tubes in present day calcrete soils, occur in phosphate horizons associ­ ated with shallowing-upwards peritidal deposits . The exact setting for their formation (supratidal or fully terrestrial) is uncertain but the remarkable similarities between these phosphatic fabrics and those of present day microbial soil carbonates must place this discovery as the strongest candidate for the earliest biologically active soil . The 'greening' of the land surface, albeit by a microbial sludge, would have begun a series of wide reaching changes in weathering and sedimen­ tary processes . Land surfaces, lacking any biological cover, are prone to erosion by wind and runoff. Even simple microbial mats on the surface would have provided some binding of weathered materials (CampbeU 1979), although roots provide a much more effective binding agent . As a result of binding, rates of erosion may have decreased and weathered materials would have had a longer residence time in the soil, allowing greater decomposition . The biological cover might also have increased levels of carbon dioxide in the soil, and would have added organic acids; both factors would have promoted chemical weathering in the soil . All these effects

V . P . WRIGHT

Introduction The soil is probably the most studied and best understood ecosystem on Earth, yet very little is known of its origins or the timings of each develop­ mental stage in its evolution . This situation arises both because of the low preservation potential of soils and through a lack of study . A variety of soils have been recognized in Pre­ cambrian sequences ranging back to over 3000 Ma . During the latter half of the Precambrian and through the Phanerozoic a gradual diversification of soil types occurred (Retallack 1986), reflecting both atmospheric evolution and biological diver­ sification, especially since Middle Palaeozoic times . Although many, i f not most, details o f the evo­ lution of soil communities and their interactions remain conjectural, several major stages can be de­ fined. The evidence, circumstantial at best, suggests that biologically active soils have existed since at least Middle Cambrian times (Fig . 1 ) .

Abiotic soils No direct evidence has been found for biologically active soils during the Precambrian, although a variety of weathering profiles and structural palaeo­ sols have been discovered (Retallack 1986) . Organic­ rich palaeosols apparently occur in the 2400 Ma Blind River Formation of Ontario (Campbell 1979) . High levels of radiation, adverse temperatures and atmospheric conditions must have prevented colonization of the land surface, even though micro­ bial life existed in the contemporaneous seas . The soils which developed during the Precambrian were the products of purely physical and physico­ chemical processes .

Microbial soils Cyanobacteria were abundant in the Precambrian, including intertidal forms which were adapted to

57

1 Major Events in the History of Life

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must have increased many-fold with the adven t of rooted vegetation . On newly exposed surfaces cyanobacteria are usually the first colonizers, followed by lichens . Fungally produced oxalic acid in lichens is a major factor in rock decomposition, but the timing of the appearance of the fungal - cyanobacterial ass oci­ ation is unclear. The vast majority of lichen-forming fungi belong to the ascomycetes, but the earliest record of these is from the Ludlow of Gotl and (Sherwood-Pike & Gray 1985) . Present day microbial soils are best developed in restricted settings which do not provide guides to

the sorts of soils possible in the past . Under suitable conditions relatively thick microbial mats may have developed, especially in humid climatic regimes . Such soils must have provided suitable micro­ climates for the first terrestrial invertebrates (Rolfe 1985; Section 1 . 8 . 3), even if the bare landscapes were still too hostile . However, no records of such microbial soil faunas are known with confidence . Highly bioturbated palaeosols have been recorded from the Late Ordovician (Ashgillian) Juniata Formation of Pennsylvania, U . S . A . (Retallack 1986) . These consist of burrows 3 - 16 mm in diameter, extending to depths of 50 cm in the now compacted argillaceous palaeosol . The burrows occur in fluvial overbank deposits, and it is often very difficult to determine if such burrows are truly those of soil dwellers or the result of burrowing during temporary subaqueous phases caused by flooding. As yet no attempt has been made to detect organic carbon isotope signatures in pedogenic carbonates in Lower Palaeozoic palaeosols, but this might prove a fruitful avenue of investigation .

Bryophyte soils By the Late Ordovician bryophytic-like terrestrial vegetation had appeared (Section 1 . 8.2). Such a veg­ etation cover, although relatively thin, would again have provided opportunities for faunal colonization . The nearest possible present day analogues for such biotas are to be found associated with lichens or moss cushions . They are characterized by a com­ munity of microarthropods, such as mites and springtails, but these only have a geological record back to the Early Devonian (Siegenian) Rhynie Chert . Could it really have taken over 40 million years for invertebrates to have colonized the bryo­ phyte 'felt' covering the land surface, a land surface which probably already had a long history of micro­ bial cover? The earliest known terrestrial faunas of the Early Devonian (Section 1 . 8 . 3) were already diversified and contain representatives of the major soil ecosystem components . The earliest evidence of a terrestrial biota, although tentative, consists of faecal pellet-like ovoid and cylindrical bodies of hyphal fragments from the Ludlow of Gotland (Sherwood-Pike & Gray 1985) . These may provide evidence of myco­ phagous feeders, and the presence of associated ascomycete fungal remains indicates that the de­ composer subsystem of the soil ecosystem had already evolved.

1 . 8 Terrestrialization Rooted soils The next major step was the development of a rooted plant cover . This happened progressively with the diversification of the vascular plants from Early Silurian times, with a further major step in late Devonian times when true forests first ap­ peared. The final stage in this series of events, at least to date, was the rise of the grasses in the Tertiary (Section 1 . 1 1 ) . The consequences of a rooted plant cover were far greater than those of a simple microbial or bryophytic one . The increased stability of the soil, and increased biomass, would have resulted in thicker soils and thicker humus. The degree of biochemical and biophysical weathering would have increased dramatically, and from Devonian times on soil-types diversified in re­ sponse to these changes (Retallack 1986) . The advent of a prominent rooted zone would have been associated with the development of the rhizosphere, with its own complex biotic inter­ actions. A critical event would have been the in­ itiation of symbiotic fungal - root relationships (mycorrhizal associations), in which the fungal component acts as a nutrient supplier to the roots . These fungal associations occur either internally within the root (endomycorrhizae) or as sheaths around the roots (ectomycorrhizae) . Occurrences of actual fungal remains with roots have been re­ corded from the Rhynie Chert and also abundantly from early Carboniferous soils, as calcification pro­ ducts of basidiomycete fungi around root tubes . In such cases, however, it is difficult to categorically establish that the fungi were not simply saprophytic forms.

Ecology The soil is an essential component of the terrestrial ecosystem, and one of its most critical functions is to decompose organic matter, making plant nutri­ ents available for recycling. The primary producer subsystem must, by all reasonable considerations, have been present from Cambrian times or earlier. The possible occurrence of fungal tubes in middle Cambrian terrestrial phosphorites of Australia, and the presence of ascomycete remains from the Ludlow of Gotland suggest that by the Middle Silurian, if not much earlier, the decomposer sub­ system had also developed . Thus recycling became possible . Possible microarthropod faecal pellets in the Silurian suggest the presence of consumers (mycophagous forms) . Some 20 million years later,

59

as revealed in the Siegenian Rhynie Chert, a fauna of spring-tails, mites, spiders, and trigonotarbid arachnids had appeared, representing many of the important components of the ecosystem (Section 1 .8 . 3) . By early Carboniferous times the soil ecosystem had evolved to a point where it produced a variety of humus fabrics identical to those found in present day soils (Wright 1987), which must reflect the action of the same types of complex biogenic processes . The evidence is frustratingly incomplete, and further work is required especially to integrate the occurrences of the early soil faunas with their associated soils . The effort needs to be made to search for evidence of biofunction in early Palaeo­ zoic terrestrial deposits, since such soils were prob­ ably organically active . What can be said, with growing confidence, is that the first vascular plants must have colonized a land surface which already had a long history of biological activity. Studies of microbial or bryophytic soils today will provide us with some clues as to the possible forms taken by these earliest soils .

References Campbell, S . E . 1979 . Soil stabilization by a prokaryotic desert crust: implications for Precambrian land biota. Origins of Life 9, 335 - 348 . Golubic, S. & CampbeII, S . E . 1979 . Analogous microbial forms in Recent subaerial habitats and in Precambrian cherts : Gloeothece coerulea Geitler and Eosynechococcus moorei Hofmann . Precambrian Research 8, 201 -217. RetaIIack, G.J. 1986. The fossil record of soils . In: V . P . Wright (ed . ) Paleosols: their recognition and interpretation, pp . 1 - 57. Blackwell Scientific Publications, Oxford . Rolfe, W.D.I. 1985 . Early terrestrial arthropods: a fragmentary record . Philosophical Transactions of the Royal Society of London B309, 207-218. Sherwood-Pike, M.A. and Gray, J . 1985 . Silurian fungal re­ mains: probable records of the Class Ascomycetes. Lethaia 18, 1 -20. Southgate, P.H. 1986 . Cambrian phoscrete profiles, coated grains, and microbial processes in phosphogenesis: Georgina Basin, Australia. Journal of Sedimentary Petrology 56, 429-441 . Wright, V.P. 1987. The ecology of two early Carboniferous soils. In : J. Miller, A . E . Adams & V.P. Wright (eds) European Dinantian environments. Special Publication of the Geological Journal No . 12, pp . 345 - 358. John Wiley & Sons, Chichester.

1 Major Events in the History of Life

60

1 . 8 . 2 Plants D . E D W A R D S & N . D . B U RG E S S

Introduction Land plants encounter problems relating to water stress, uptake, and transport, and to aerial dispersal of propagules . Survival in such habitats is associated with three major strategies : 1 Drought avoidance via opportunism and ephemeral life cycles completed under favourable conditions . 2 Extreme desiccation tolerance involving the capacity of cytoplasm to rehydrate and then function normally (poikilohydry) . 3 Maintenance of an internally hydrated environ­ ment by biochemical and anatomical modifications (homoiohydry) . Extant land vegetation includes representatives of all major groups; cyanobacteria, algae, bryo­ phytes and tracheophytes. The last are usually considered most successful and are homoiohydric possessing xylem (with lignin) for water transport, a waxy cuticle (cutin) for reducing evaporation, sto­ mata and an intercellular space system for gaseous transport (Raven 1984) . The poikilohydric life style of cyanobacteria, algae, and bryophytes is usually considered more primitive, is of particular signifi­ cance in the colonization of unstable environments, and hence would have been important in pioneering land plants . The preservation potential of land plants is linked to these strategies in that cutin and lignin are dur­ able and may persist, albeit modified, in fossils, but in poikilohydric forms, the only parts which might be expected to be fossilized are resting stages and/or dispersal units such as spores. The latter, impregnated with sporopollenin, a complex fatty polymer, also occur in tracheophytes . Thus although there is no direct record of thallophytes (cyano­ bacteria and algae) colonizing moist land surfaces in the Early Palaeozoic, it seems likely that they were present. A possible limiting, physical factor may have been high ultraviolet (UV) radiation cor­ related with low atmospheric oxygen . Indeed it has been postulated that lignin evolved from precursors involved in UV absorbance, and that cutin and sporopollenin initially had a similar role in UV reflectance . With regard to higher plants, attempts to demon­ strate the vascular status of megafossils, thus pro-

viding unequivocal evidence for land vegetation, have traditionally dominated research . However, more recently the affinities of Ordovician and Silurian microfossils have been rigorously appraised in the search for alternative pioneering colonizers . The first records and ranges of all fossils thought relevant to terrestrialization are documented in Fig . 1, and numbers below refer t o that figure .

Sporomorphs

1, 2 . Cryptospores . (lacking trilete ( Y ) or monolete

( I ) marks; after Richardson & Edwards 1989. )

Obligate permanent tetrads (1), so named because they do not split into four spores (monads) on dispersal, possess durable, smooth, unornamented walls thought to be impregnated with sporopol­ lenin, although this has not been chemically proven. They are thus considered to derive from land plants . Those characterizing Upper Ordovician spore as­ semblages are smaller, smooth walled, and often lack the enveloping smooth or sculptured 'mem­ brane' typical of most early Silurian forms . Its ab­ sence may result from poorer fossilization potential. Such tetrads increase in numbers and diversity, dominating assemblages until the end of the Llandovery. Thereafter they become relatively less common and occur only rarely in Lower Devonian sediments, where they are probably reworked . Gray (1985) has argued most persuasively that as com­ parable tetrahedral tetrads (sometimes membrane enclosed) occur in certain living liverworts, they thus derive from poikilohydric plants with bryo­ phyte physiology and life histories . It is also pos­ sible that they belonged to freshwater or marine algae for which there are no modern analogues, or that they were shed by intermediate extinct forms that lived in ephemeral water bodies producing spores when these dried up . Membrane enclosed monads and obligate dyads (2) have similar ranges to tetrads and were probably of similar derivation. 3 . Dyads. Habitually lacking a membrane, and be­ lieved to split into the consistently associated alete (lacking trilete or monolete marks) spores with thinner proximal faces and identical distal features, these are distally smooth walled in earliest records (Rhuddanian) and sculptured from the Homerian . They persist throughout the Silurian and are rela­ tively common in basal Devonian assemblages . Dyads occur in Salopella-like sporangia in the Pffdoli . The affinities of that genus remain

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62

1 Major Events in the History of Life

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Hostinella) Associated with the earliest tet­

tracheids

possess a central strand composed of

(14), but whether or not pre-Ludlow repre­

rads are small cuticular fragments, thought ana­

sentatives were vascular is unknown. Some may

logous to vascular plant cuticles . They lack stomata

derive

and are usually imperforate, with smooth ?outer

tracheids had not yet evolved, while others may

from

plants

of

small

stature

in which

surface . Ornamented forms appear in the Wenlock

possess conducting tissues of bryophytic nature (cf .

and continue into the Gedinnian . A reticulate pat­

Lower Devonian

tern represents the outlines of surface cells in the

exhibits many homoiohydric characters, and would

underlying tissue . In

Nematothallus,

such cells were

± isodiametric in tangential section, while in the

cuticles of higher plants they are elongate vertically . Lang (1937) suggested that they covered

thallus,

Nemato­

a thalloid plant composed of tubes which he

placed in the Nematophytales

(15, 1 6),

a taxon for

plants with organization neither algal nor higher

Aglaophyton (Rhynia) major

which

be assigned to the Tracheophyta but for the moss­ like conducting tissues) .

1 0 - 1 3 . Fertile tracheophytes. Wenlock Cooksonia (Rhyniophytina: 1 0) is generally accepted as the

earliest erect pteridophyte-like plant (Edwards

et al.

1983) . Reservations as to its affinity stem from a complete lack of anatomy . Spores occur in PHdoli,

plant . While there may be some doubt that all durable

and stomata and sterome in Gedinnian

C. pertoni.

spores derive from land plants, this is not the case

Tracheids have never been demonstrated in central

for cuticles, although being imperforate and hence

strands .

relatively impermeable to gases, their function and

Steganotheca

even composition in Nematothallus might have been different from that in tracheophytes, e . g . primarily

to later examples, e . g .

as UV screens, facilitating runoff, or in defence . It is

Thus although

Cooksonia, Salopella

and

are usually assigned to the Rhynio­

phytina because of general morphological similarity

Rhynia gwynne-vaughanii,

they are better called 'rhyniophytoid' to emphasize

unlikely that they belonged to the tetrad producers

our ignorance . A major radiation is recorded in the

because, although the first records are coincident,

early Gedinnian, but they then became insignificant

cuticles persist into the Emsian and are sometimes

constituents of land vegetation (Edwards & Fanning

quite common constituents of Lower Devonian

1985) .

assemblages .

7, 8. Higher plant cuticles.

Baragwanathia

longifolia

(1 1 )

in

Australian

Ludlow strata is morphologically similar to Lower Homerian fragments with

Devonian examples, with sufficient anatomical as

larger, more strongly demarcated and aligned cells

well as morphological characters to indicate lyco­

are interpreted as sporangial from comparison with

phyte affinity. Thus, even in the absence of anatomy

dispersed and

in Silurian representatives, its vascular status is un­

in situ

Gedinnian rhyniophytoid

examples (1 0) . Cuticles without stomata deriving

questioned .

The earliest lycophyte with typical

1 . 8 Terrestrialization sporangium/sporophyll organization is the late Emsian Leclercqia . Zosterophyllum myretonianum (12) is the earliest fertile member of the Zosterophyllophytina, al­ though there are records of its characteristic branch­ ing (K- and H-shaped) in sterile Pffdoli axes. The first major zosterophyll radiation is recorded in the late Gedinnian of south Wales. Dawsonites sp . (13), a fragment of a fertile truss of Psilophyton in the south Wales Siegenian, marks the beginnings of the Trimerophytina. The Ludlow Australian record is less convincing. The trimerophytes diversified rapidly in the Emsian and are considered ancestral to ferns s.l., progymnosperms and sphenopsids .

Nematophytales

15. Microfossils of tubular organization, either as iso­ lated tubes or wefts, are recorded from the Telychian into the Lower Devonian . The most conspicuous tubes are internally sporadically thickened ('banded'), broadly resembling tracheids in their ornament, but there is no direct evidence that they were lignified . The source plants are problematic: they occur with smaller tubes in Nematothallus (Lang 1937) and have been found in plants with organi­ zation otherwise typical of Prototaxites (16). The habitats of such organisms, be they freshwater or terrestrial, remain as conjectural as their affinities . In that some tubes (but not banded forms) have been recorded attached, rather than just adpressed to cuticles of Nematothallus (6) type, they may well derive from land plants . Further isolated examples include tubes with smooth thick or thin walls, or filaments (occasionally branched) composed of elongate, narrow cells . The latter frequently occur in monotypic wefts or may be associat� d with wider smooth or banded tubes . Some of the associations may belong to Nematothallus or Nematoplexus . 1 6 . Prototaxites (Wenlock- Upper Devonian) is included because it is sometimes cited as a land plant largely due to its occurrence in tracheophyte assemblages in freshwater sediments . Its organi­ zation, in which narrow filaments enclose wider smooth tubes, is unique, and hence in the absence of reproductive organs its affinities, possibly algal or fungal, remain unknown, and speculation on the functions of its tissues unrewarding. 1 7. Parka, best known from the Scottish Gedinnian, a possible epiphyte in lacustrine habitats, may have

63

some relevance to the ancestry of higher plants in that it has been compared with the charophycean Coleochaete, although the latter lacks the cavities with numerous alete spores found in Parka. Com­ parative biochemical and ultrastructural studies suggest that among the green algae the Charo­ phyceae show closest similarities with bryophytes and tracheophytes while Coleochaete, with its parenchymatous organization, and protection, nutrition, and prolonged retention of the zygote, possesses the greatest number of advanced features .

18. Pachytheca i s exceedingly common in certain marginal fluviatile and lacustrine facies in the Lower Devonian . Its frequent association with Prototaxites has led to the suggestion that it was involved in its vegetative reproduction . However, the fossils suggest that the organism comprised a sphere of a mucilage-like substance in which filaments of cyanobacterial dimensions were embedded. Its habitat is interpreted here as freshwater, possibly littoral lacustrine . 19. Fungi. Although not considered plants, fungi are included here because it has been suggested that initial terrestrialization was possible only after the development of a symbiotic association between a semiaquatic green alga and an aquatic oomycete fungus, and that in the colonization of nutrient­ poor environments the fungus would have ex­ ploited large volumes of substrate for minerals (cf. mycorrhiza today) . Resting spores of presumed mycorrhiza in some Rhynie Chert axes are fre­ quently cited as supporting evidence, but the abundant spheres and hyphae may just indicate saprotrophism (i . e . decomposition of dead organ­ isms) in peat development. Further evidence for terrestrial fungi is the record of ascomycetes remains (hyphae, probable conidia, and ascospores) from the Ludlow of Gotland (Gray 1985), and similar, but more poorly preserved, material from the late Llandovery . Terrestrial vegetation It is postulated that moist land surfaces in the early Palaeozoic would have been coated with a green scum, perhaps initially of cyano- and eubacteria, later joined by filamentous and unicellular algae . Such an encrusting layer would have both physically stabilized and chemically broken down the sub­ strate, releasing nutrients and, in stable environ­ ments, resulting in the build-up of humus (see also

64

1 Major Events in the History of Life

Section 1 . 8 . 1 ) . From the middle Ordovician onwards microfossils morphologically convergent with those from later tracheophytes suggest a novel vegetation, possibly with thalloid organisms covered by cuticle and spore producers with liverwort life-style; aerial dispersal indicates the attainment of some stature . The appearance of Ambitisporites in the Llandovery heralded a new phase - the advent of pteridophyte­ like plants with axial organization, possibly forming a 'turf' just a few centimetres high . The larger size permitted by homoiohydry, the concomitant main­ tenance of turgor and hence a hydrostatic skeleton, conferred potential superiority over poikilohydric forms in terms of wind dispersal of propagules and in shading, thus limiting the productivity of smaller forms . Throughout the late Silurian there is an increase in axis diameter and length of fragments : sprawling Baragwanathia probably formed thickets . Lower Devonian assemblages suggest that many of the tracheophytes grew in monotypic stands, exten­ sive cover resulting from prolonged rhizomatous activity. Such plants would have provided mutual support - some of the Emsian trimerophytes attained a height of over 1 m. As to habitats, the best direct evidence comes from the Rhynie Chert, but as all these early pteridophytes were homo­ sporous (i . e . with spores of one size), the free-living gametophyte would have required moist conditions both for vegetative growth and reproduction . With regard to route of terrestrialization for higher plants, physiological considerations support transmigration from fresh water on to land .

References Edwards, D . 1980 . Early land floras . In: A.L. Panchen (ed . ) The terrestrial environment and the origin of land vertebrates . Systematics Association Special Volume 15 pp. 55 - 85 . Academic Press, London. Edwards, D. & Fanning, V. 1985 . Evolution and environment in the late Silurian-early Devonian: the rise of the pteri­ dophytes . Philosophical Transactions of the Royal Society of London B309, 147 - 165 . Edwards, D . , Feehan, J . & Smith, D . G . 1983 . A late Wenlock flora from Co. Tipperary, Ireland. Botanical Journal of the Linnean Society 86, 1 9 - 36 . Fanning, V . , Richardson, J.B. & Edwards, D. 1988. Cryptic evolution in an early land plant. Evolutionary Trends in Plants 2, 13-24. Gray, J . 1985. The microfossil record of early land plants : advances in understanding of early terrestrialization, 1970- 1984. Philosophical Transactions of the Royal Society of London B309, 167-195. Lang, W.H. 1937. On the plant remains from the Downtonian of England and Wales. Philosopical Transactions of the Royal Society of London B227, 245 - 291 .

Raven, J.A. 1984. Physiological correlates of the morphology of early vascular plants. Botanical Journal of the Linnean Society 88, 105 - 126. Richardson, J.B. & Edwards, D . 1989 . Sporomorphs and plant megafossils. In: CH. Holland & M . G . Bassett (eds) A global standard for the Silurian System, Geological Series No . 9, pp . 216-226. National Museum of Wales, Cardiff.

1 . 8 . 3 Invertebrates P . A . SELDEN

Introduction The diversity of invertebrate species on land greatly exceeds that in the sea; this is almost entirely due to the terrestrial insects which form 70% of all animal species alive today . However, of over 30 invertebrate phyla, only the arthropods, the molluscs, and the annelids have significant numbers of macroscopic terrestrial representatives . A greater number of phyla include very few terrestrial species, crypto­ biotic representatives, or internal parasites on terrestrial organisms . The body plans of some highly successful marine phyla have apparently precluded their terrestrialization; these include the sipunculid, echiuroid, and priapulid worms, cnidarians, lophophorates, chaetognaths, pogonophores, hemi­ chordates, and echinoderms . No phylum originated on land, and no major terrestrial taxon has become extinct, as far as is known . Outstanding questions on terrestrialization are : what physiological mechanisms enabled inver­ tebrates to emerge onto land; did each taxonomic group use similar mechanisms; were their routes onto land the same; did they all come onto land simultaneously, suddenly or gradually, or in dif­ ferent invasions? The hardest evidence comes from comparative physiology, but palaeontology has the power to test theories based on living material, and uniquely adds the dimension of time . Invertebrates moving from seawater to land ex­ perience profound changes in all aspects of life (Little 1983) . On land, water supply is at least vari­ able, and commonly seasonal . To invertebrates, whose air breathing mechanisms utilize diffusion to a far greater extent than ventilation, oxygen is more available in air than in water because the diffusion coefficient (partial pressure per unit length, in ml/[min x cm2 x cm x atm]) of oxygen in

1 . 8 Terrestrialization water is 0 . 000034, but in air is 1 1 . 0 . Support is more problematical in the less viscous aerial medium than in water, but once overcome, locomotion is easier and faster. The difference in refractive index between air and water poses a problem for visual sense organs in transition, but high frequency vibrations can be perceived more easily in air, resulting in a greater use of sound by terrestrial invertebrates . On land, internal fertilization is the norm, and greater protection (e . g . from drought) is afforded to the developing embryos . Changes in nutrition, ion balance regulation, and excretion are also necessary for terrestrialization . Some land animals avoid the difficulties of water supply by living in soil interstitial water; strictly, such animals (e . g . protozoans, ostracodes, and nematodes) should not be regarded as terrestrial . Poikilohydry i s used only b y small terrestrial animals, such as protozoans, tardigrades, nema­ todes, and rotifers, whose habitat is subject to seasonal drought periods . Many soil, litter, and crevice dwellers are able to take advantage of the high humidity in such habitats, and though they are often able to foray in drier situations (e .g. wood­ lice across the kitchen floor), retreat to the. humid home base is essential to prevent desiccation . In addition to woodlice, the centipedes, millipedes, flatworms, leeches, and earthworms are included in this group . Some animals, such as many land snails, can withstand desiccation during dry periods by aestivation, but require water or high humidity for activity at other time s . Finally, the true invertebrate conquerors of the terrestrial habitat, not requiring a humid environment in which to flourish, but active in dry, and even desert, conditions, are the majority of insects, many arachnids, and a few crustaceans . All terrestrial arthropods have waterproofing in the cuticle, but the form this takes differs in each arthropod group and is not always well studied. The differences may be important for palaeontology, however, since the preservation potential for differ­ ent cuticles is not the same .

The fossil record The fossil record of terrestrial invertebrates is shown in Fig. 1 (Rolfe 1980; Chaloner & Lawson 1985) . There is no fossil record of terrestrial flatworms, nemerteans, or nematodes, although fossil examples of parasitic and aquatic nematodes are known (Conway Morris 1981) . Oligochaete annelids are known from the Carboniferous . Their traces, in-

65

cluding burrows and faecal pellets, occur in palaeo­ sols from the Carboniferous onwards . They may have emerged onto land with the first humic soil (Section 1 . 8 . 1 ) . Land snails, both helicinid prosobranchs and stylommatophoran pulmonates, are recorded from the Upper Carboniferous, indicating that they had already become significant members of the land fauna by that time . The earliest basommatophoran pulmonate is Late Jurassic in age; this contradicts evidence from comparative morphology, which suggests that basommatophorans were ancestral to the other pulmonates . Possibly the development of ground shade and deciduous leaf litter (probably Lower Carboniferous) was necessary before land snails could be assured of the damp conditions necessary for colonization (Solem 1985) . All extant insects are terrestrial or secondarily aquatic, and there were no terrestrial trilobites, as far as we know. The record of Onychophora, which includes the Recent Peripatus, appears to begin with Aysheaia from the marine, Middle Cambrian Burgess Shale . Terrestrial uniramians (myriapods and insects) were thought to have evolved from land-living onychophorans, but there is new evi­ dence that the earliest myriapods were marine . This comes from myriapod-like fossils in marine sedi­ ments from the Silurian of Wisconsin and the Middle Cambrian of Utah . By the Devonian, milli­ pedes, centipedes, and arthropleurids had appeared in terrestrial faunas, and some reached giant pro­ portions in the Carboniferous forests . The earliest apterygote insects occurred in the Devonian, but the first pterygotes were Carboniferous in age . Eurypterids ranged from Ordovician to Permian and were predominantly aquatic animals, but from the Silurian onwards some were amphibious, as evidenced by their accessory lungs . They illustrate a failed attempt at terrestrialization using a method now being tried by the Crustacea. Their close rela­ tives, the scorpions, succeeded however, by changing their gills into lungs . All other arachnids are primarily terrestrial today, and the evidence from comparative morphology suggests that each arachnid group emerged onto land independently. The oldest are the trigonotarbids : extinct, close rela­ tives of spiders, with good terrestrial features, from the Lower Devonian of Rhynie, Aberdeen . In the Devonian are also found mites, pseudoscorpions, and possibly spiders, and by the Carboniferous there were more arachnid orders than today; only the spiders have radiated more dramatically in later periods .

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1 . 8 Terrestrialization The fossil record of crustaceans is generally good because, like the trilobites, they have a mineralized exoskeleton . However, the terrestrial groups show very short fossil ranges. The first amphipods are Upper Eocene, although it has been suggested, on biogeographical grounds, that their origins lie in the Middle to Late Mesozoic at least. The terrestrial talitrids, with no fossil record, are considered by some to have emerged onto land when the first angiosperm forests became established in coastal regions . The isopods have a long fossil record, from the Upper Carboniferous, with their supposed origins in the Devonian, but the terrestrial Oniscoidea are known only since the Eocene . Al­ though crabs and crayfish first appeared in the Jurassic, the important crab radiations did not occur until the Cretaceous and the Eocene; families with terrestrial representatives first appeared in the Palaeogene, but true terrestrial forms not until the Late Neogene .

Morphological adaptations for life on land A major problem for terrestrializing animals is that both oxygen and carbon dioxide molecules are larger than the water molecule, so that any membrane across which the respiratory gases are diffusing will leak water . This may not be too disastrous in moist environments like the soil, in which animals such as earthworms can use cutaneous respiration, but inhabitants of dry habitats need a waterproof skin and have developed special respiratory organs to reduce water loss. Respiratory organs can be broadly classified into gills, (evaginations) used primarily in water and lungs (invaginations used primarily in air) . A great many animals utilize cutaneous gas exchange in conjunction with gills or lungs. Aquatic animals which venture onto land for short periods of time may use their gills for air breathing, but if much time is spent on land, access­ ory lungs are usually developed . Many examples of animals with both lung and gill can be found among the gastropods and the Crustacea . In some instances, the lung developed not for land life, but to withstand poorly oxygenated water or drought periods (cf. lungfish) . True lungs among the invertebrates are found only in gastropod molluscs and arthropods . Among gastropods the pulmonates (land snails and slugs), and a few prosobranchs (e . g . helicinids), are the only truly terrestrial forms . The gastropod lung is formed from a highly vascularized part of the mantle cavity, which in pulmonates opens by a small pore

67

(the pneumostome) to the outside . In the arthro­ pods, book-lungs, tracheae, and pseudo tracheae are all types of lung which have evolved independently in a number of groups. The book-lungs of arachnids are homologous with the gills of the aquatic chelice­ rates, and appear to have been derived from them simply by sealing the edges of the gill covers and leaving a hole (the stigma) to connect to the outside . The early scorpions (Silurian to Carboniferous) were aquatic and gills are known in the Devonian Waeringoscorpio from Germany; but by the Lower Carboniferous, pulmonate scorpions had appeared alongside the aquatic forms . In the related, extinct eurypterids, the so-called gills actually resemble some crustacean air-breathing organs, which suggests that this was their real function, and that true gills, being thin membranes, have not been preserved or recognized in fossils . As in the pul­ monate gastropod lung, dendritic structures resem­ bling insect tracheae have developed within the book-lungs of some arachnids; additionally, some arachnid groups have developed tracheal systems. Among the chelicerates, therefore, respiratory organs developed independently in each group by modification of various pre-existing organs accord­ ing to need . The insect tracheal system is a dendritic pattern of tubes arising from apertures (spiracles) in the body wall, and penetrating to every tissue in the body to supply oxygen directly to the cells . Since the insects appear to have evolved from terrestrial myriapods, the problems of terrestrialization have never troubled them, which may explain their success . A variety of tracheal systems occurs among the myriapod groups . Several independent terrestrial lines are found in the Crustacea (Powers & Bliss 1983), principally the talitrid amphipods, the isopods, and the land crabs . In the land crabs, secondary lungs are developed that work alongside the gills (which are never lost) . The isopods are more terrestrialized than the crabs, and their pleopods (gills) bear invaginations (termed pseudo­ tracheae, from their resemblance to insect tracheae) for air breathing . For small animals, hydrostatic skeletons work as well on land as in water; witness the success of the slug form. Arthropods moving onto land evolved the hanging stance for stability, and additionally use some form of leg 'rocking' or jointing mechan­ ism to prevent the plantigrade foot from twisting on the ground (with consequent abrasion and loss of grip) during walking; such features can be seen in fossils . Arthropods become vulnerable during

68

1 Major Events in the History of Life

moulting, and it is possible that pioneer terrestrial forms returned to the water for ecdysis . Sense organs on fossils can give clues to terrestriality: tricho­ bothria (fine hairs which respond to air vibrations) found on Devonian arachnids prove their terrestrial mode of life, and stridulatory organs on the same animals at least suggest it . Complex copulatory organs preserved in fossils suggest a terrestrial habitat and their absence is evidence for an aquatic life .

Routes onto land The physiological barrier between sea and land can be crossed by a number of route s . Invertebrates which moved onto land across the marine littoral environment include the talitrids, the isopods, and most crabs, within the Crustacea, and possibly the chelicerates and the uniramians . There is evidence that some terrestrial forms emerged via brackish water (some crabs) or salt marshes (some pulmonate snails ) . The freshwater route was used by the oligochaetes, leeches, prosobranch gastro­ pods, and the burrowing potamonid crabs and cray­ fish . Intex:stitial forms have utilized both fresh- and salt water routes, and it is possible that the very earliest land animals followed this route . Indeed, a late Ordovician palaeosol from Pennsylvania is full of coprolite-bearing burrows which have been attributed to the activities of microarthropods, possibly myriapods (Section 1 . 8 . 1 ) . From the fragmentary record, i t would appear that most terrestrial invertebrates arrived on land with, or shortly after, the Silurian plant invasion (Section 1 .8 . 2) . The first records are of fully adapted land animals (the Rhynie Chert of Aberdeen, the Alken fauna of Germany, and the Gilboa fauna of New York), which points to a pre-Devonian terrestrialization period for most groups . The major exception is the Crustacea, which are attempting terrestrialization now . The pressures, or advantages, which cause terrestrialization are undoubtedly various (e . g . escape from predators, more abundant food supply) and invite speculation . What is clear, however, is that animals came onto land together with their biotic interactions, and hypotheses should seek to explain the invasion of the land by biotas rather than individual taxa .

References Chaloner, W . G . & Lawson, J . O . (eds) 1985 . Evolution and environment in the Late Silurian and Early Oevonian.

Philosophical Transactions of the Royal Society of London B309, 1 -342 . Conway Morris, S. 1981 . Parasites and the fossil record . Parasitology 82, 489 - 509 . Little, C . 1983 . The colonisation of land. Cambridge University Press, Cambridge . Powers, L.W. & Bliss, O . E . 1983 . Terrestrial adaptations. In: F.J. Vernberg & W.B. Vernberg (eds) The biology of Crustacea, Vo! . 8, pp. 271 - 333. Academic Press, London. Rolfe, W.O.I. 1980 . Early invertebrate terrestrial faunas. In: A.L. Panchen (ed . ) The terrestrial environment and the origin of land vertebrates . Systematics Association Special Volume 15, pp. 117- 157. Academic Press, London. Solem, A . 1985 . Origin and diversification of land snails. In: E.R. Trueman & M.R. Clarke (eds) The mollusca, Vo! . 10, pp . 269-293. Academic Press, London .

1 . 8 . 4 Vertebrates A . C . MILNER

Introduction The earliest terrestrial radiation is presumed to have been of fish-like tetrapods (four-legged land ver­ tebrates - amphibians, reptiles, birds, and mam­ mals) capable of moving on land and breathing air. Modification of structure, function, and physiology in subsequent radiations led to a monophyletic group of truly terrestrial vertebrates, the amniotes . The amniotes comprise two sister groups : ther­ opsids, which include mammals; and sauropsids, which include reptiles and birds . Amniotes evolved a totally terrestrial life cycle, eliminating an indepen­ dent aquatic larval phase by means of a relatively waterproof extraembryonic membrane (amnion) which encloses the developing embryo in fluid, and a shelled egg . This reproductive strategy enabled colonization of the terrestrial environment, and early amniotes diversified into lineages leading ulti­ mately to mammals and birds.

The earliest tetrapod record Tetrapod remains first appear in the fossil record in the Frasnian stage of the Upper Devonian. The only abundant skeletal remains are those of the ichthyo­ stegalians, discovered in the nineteen-thirties in the Famennian red beds of East Greenland (Jarvik 1980) . Three genera have been recognized, Ichthyostegopsis

1 . 8 Terrestrialization from skulls only, and Acanthostega and Ichthyostega from skull and postcranial material, although no complete skeleton has been described (Fig. 1 ) . Ichthyostega i s undoubtedly the most primitive tetrapod known and retains many fish-like characters . Specialized autapomorphies debar it from direct ancestry of all other tetrapods .

Tetrapod - fish relationships The orthodox view of the origin of tetra pods is that they derive from one particular group of bony fishes (Osteichthyes), the osteolepiforms, which are all fossil . This is currently in dispute and the subject of major contradictory reviews . Rosen et al. (1981) have argued that lungfish (Dipnoi) are the sister group of tetrapods, based on the shared derived character of a choana (internal nostril) and other support­ ing homologies . Panchen and Smithson (1987) reappraised the same data and concluded that lung­ fish do not share a true tetrapod choana; they support the traditional view that osteolepiform fishes are the sister group of tetrapods and, there­ fore, that the extinct taxa contained in that group are more closely related to tetrapods than are the lungfish . Both osteolepiforms and dipnoans first appear in the Lower Devonian and if either is the sister group of tetrapods then the earliest tetrapods must also have been present in the Lower Devonian (Bray 1985; Milner et al. 1986) . It is now generally accepted, however, that the tetrapods are monophyletic . A diphyletic origin from two separate groups of fossil osteichthyan fishes has been proposed by Jarvik (1980) . His theory derives living urodeles (salaman­ ders) from porolepiforms, and all other tetrapods (amphibian and amniote) from osteolepiforms;

Fig. 1 Composite skeletal reconstruction and flesh restoration of lchthyostega, the most primitive terrestrial tetrapod known. Length about 65 cm; the largest specimens attained a length of about 1 m. (From Jarvik 1980 . )

69

it has not received support outside the Swedish school .

Morphological adaptations for life on land The classical scenario painted a picture of terrestrial vertebrates emerging onto land from freshwater, argued on physiological grounds . Such a transition was thought to be in response to periodically arid environments, as interpreted from the sedimen­ tology of the Devonian red beds . Recently, a number of authors (references in Bray 1985) have argued that the geological evidence favours a marine origin both for vertebrates as a whole and for tetrapods . Devonian osteichthyans are mainly associated with marine or nearshore continental environments and, indeed, the ichthyostegalians may be associ­ ated with coastal tidally-influenced sediments (Bray 1985) . Air breathing, by means of internally positioned inflatable airsacs with moist linings (lungs), is a basic character for osteichthyan fishes found also in tetrapods. It may also have been, primitively, an adaptation to the marine environment for all jawed fishes (gnathostomes) (Bray 1985) . Ureotelic ni­ trogenous excretion (production of urea to minimize osmotic dehydration) is found primitively in marine vertebrates . Thus two important physiological ad­ aptations to the terrestrial environment, air breath­ ing and the ability to cope with dehydration, were already present in the osteichthyan fishes from which tetrapods evolved . A n alternative and completely opposite scenario then, is that the environmental pressures leading to terrestrialization might have been the drive to escape from freshwater influx (and the inherent physiological problems of maintaining water

70

1 Major Events in the History of Life

balance in hypo-osmotic conditions) into shallow marine environments during a wet season (Bray 1985) . Major structural and functional adaptations are implicated in the terrestrialization of vertebrates, among them modifications of the systems involving movement and support, sensory perception, and reproduction . A complex of limb and limb girdle characters, autapomorphic for tetrapods (Rosen et al . 1981; Panchen & Smithson 1987) reflect the interwoven functions of supporting body weight and trans­ mitting muscular locomotor forces to the distal regions of the limbs . Ichthyostega, which inevitably serves as the primitive tetrapod model, displays the following characters which demonstrate the acquisition of fully functional walking limbs and sprawling gait (Jarvik 1980) : pelvic girdle connected to the vertebral column; form of the jointed limbs with a hinge joint at the wrist and knee and a rotary ankle joint; and load bearing digits with articulated phalanges (Fig . 1 ) . The derivation of the tetrapod limb from the fin skeleton of either a lungfish, as argued by Rosen et al. (1981), or an osteolepiform, preferred by Panchen & Smithson (1987), presents complex problems of homology which cannot be resolved satisfactorily from the present fossil record . The ability to receive airborne sound is an impor­ tant adaptation to life on land . Tetrapod autapo­ morphies in the middle ear, namely the presence of a fenestra ovalis in the otic capsule (part of the braincase housing the semicircular canals of the inner ear) and a stapes (an unsutured rod-like bone providing a connection between the otic capsule and the body wall) indicate that early land ver­ tebrates were able to receive low frequency airborne or water-borne sound . Structural adaptations to receive and process high frequency sound, with a slender stapes acting as a sound conductor in an impedence-matching middle ear, had developed by Visean times in temnospondyl amphibians (from which modern amphibians derive) . An impedence­ matching middle ear developed independently in amniotes and is observed first in some Permian forms . The configuration of the ear region offers clues to the evolutionary transition from amphibians to rep­ tiles (i . e . amniotes) . Soft structure autapomorphies are not reflected in the skeleton of early land ver­ tebrates that were related to amniotes; they cannot be categorized satisfactorily on skeletal characters . The relative size of the semicircular canals (organs of hearing and balance in the inner ear), proportion-

ally much larger in small animals, led Carroll (1970) to propose that the transition from an amphibian (non-amniotic) to a reptilian (amniotic) reproduc­ tive pattern occurred through a filter of small adult body size . Reproductive patterns of living terrestrial amphibians suggest that there was an intermediate stage in the development of terrestrial reproduction when non-amniote eggs were laid on land . Non­ amniote eggs are restricted in size for physiological reasons, imposing in turn a strict limit on adult body size (Carroll 1970) . It is also a recognized reproductive strategy for small terrestrial amphibians to produce a small number of relatively large yolky eggs . This permits the offspring to reach an advanced stage before hatching and is a more efficient energy investment in small forms . What­ ever the underlying cause, the process of minia­ turization involved remodelling of the skull and braincase to accommodate the still relatively large semi-circular canals . Thus the structure of the ear region is fundamentally different in amniotes and anamniotes . The earliest tetrapod that can b e unequivocally characterized as an amniote, Hylonomus, is Westphalian (Middle Silesian) in age . It possesses a suite of characters highly adaptive for a fast-running small insectivore, including slender limbs and long, slender manus (hand) and pes (foot) . It might there­ fore be concluded that this condition represents the primitive amniote ecological niche . However, a recent review of early amniote relationships con­ cluded that the early amniote ecological niche was filled by small, slow-moving general invertebrate feeders (Heaton & Reisz 1986) . There is a striking correlation between the appearance of slenderly­ built cursorial insectivores, exemplified by Hylonomus, in the late Carboniferous and the in­ creasingly diverse fauna of running and flying insects .

Early tetrapod biogeography and ecology In addition to the ichthyostegalians, the geographi­ cal range of Devonian forms has been extended recently by discoveries of tetrapod footprints from the Frasnian Stage in Australia and from the Upper Devonian in Brazil . A possible tetrapod lower jaw is also known from Australia and a partial skeleton, unequivocally tetrapod and more advanced than the ichthyostegalians, has recently been described from the Upper Famennian of European Russia (Milner et al. 1986) . The Upper Devonian tetrapod

1 . 8 Terrestrialization

71

2 The world in A, Tournaisian - Namurian and B, Westphalian time, showing the known range of fossil tetrapods (stippled) in relation to contemporaneous continental positions . (After Milner et al. 1986 . )

Fig.

record is thus very sparse; it demonstrates that tetrapods were present by the late Devonian in the palaeoequatorial regions of Euramerica and Gondwanaland but information on structural and ecological diversity is lacking. Our knowledge is likewise restricted geographi­ cally and ecologically during the Carboniferous . For discussion of the tetrapod record, the Carboniferous is most usefully divisible into two coherent units (Milner et al . 1986) . In the TournaisianlVisean/ Namurian (360 -315 Ma) most of the dozen or so families recognized are of large specialized aquatic forms, and a few specimens of small terrestrial tetrapods hint at almost unrepresented terrestrial faunas. All the tetrapods known from this period occur in a band across the southern coastal region of Euramerica from Iowa to West Germany (Fig. 2A) and most derive from lake-bed or estuarine deposits, hence the predominance of specialized aquatic forms. A recently discovered Scottish Dinantian terrestrial fauna (Milner et al. 1986), albeit very late Visean in age, is revealing a wider structural diver­ sity among terrestrial tetrapods and increases the probability that they were already structurally and ecologically diverse in the late Devonian . All Westphalian tetrapod faunas known, with the exception of one trackway recorded from the late Carboniferous of Chile, also derive from the south­ ern margin of Euramerica in a slightly wider longi­ tudinal belt from Arizona to Czechoslovakia (Fig. 2B) . Some 30 families are recognized, apparently an explosive increase in diversity compared with the pre-Westphalian record . However, this phenom­ enon is an artifact of the existence of a few highly productive Westphalian localities which represent three major environments and tetrapod associations (Milner et al . 1986) . These are : (1) an open-water fish-dominated habitat with specialized lake dwel-

ling tetrapods; (2) a swamp pool association, a pond-like environment where small amphibians predominated but with occasional lake and terres­ trial erratics; and (3) terrestrial associations found as erratics in swamp pools, deltaic fans or as the major assemblages in burnt hollow upright lycopod stumps. This last preservation, from sites in Nova Scotia, has yielded remains of small animals that had been either entrapped or used the stumps as refuges . These animals show obvious terrestrial adaptations and they include the earliest known reptile, Hylonomus (Milner et al . 1986) . It is evident from the above brief survey that virtually all that is known of the first quarter of tetrapod history (374 - 296 Ma) derives from an ap­ parent succession of faunas in a geographically re­ stricted area - the southern equatorial coastal belt of the Euramerican plate . This has been interpreted variously as the centre of origin and diversification of terrestrial vertebrates, and as the result of a concentration of collecting activity in Europe and North America. Likewise it appears, from literal interpretation of the fossil record, that the origin and early radiation of terrestrial vertebrates was a chronological sequence of faunas evolving in re­ sponse to environmental changes . The record may equally represent local succession of ecological communities along the southern coast of Eur­ america . The poverty of the fossil record in the Devonian and Carboniferous severely restricts our perspective on these problems .

References Bray, A.A. 1985 . The evolution of the terrestrial vertebrates : environmental considerations . Philosophical Transactions of the Royal Society of London B309, 289 - 322. Carroll, R.L. 1970. Quantitative aspects of the amphibian-

1 Major Events in the History of Life

72

reptilian transition. Forma et Functio 3, 165 - 178. Heaton, M.]. & Reisz, R.R. 1986. Phylogenetic relationships of captorhinomorph reptiles. Canadian Journal of Earth Sciences 23, 402-418. ]arvik, E . 1980. Basic structure and evolution of vertebrates, Vols 1 and 2. Academic Press, London . Milner, A.R., Smithson, T.R., Milner, A . C . , Coates, M . 1 . & Rolfe, W.D.1. 1986. The search for early tetrapods. Modern

Geology 10, 1 -28 . Panchen, A . L . & Smithson, T.R. 1987. Character diagnosis, fossils and the origin of tetrapods . Biological Reviews of the Cambridge Philosophical Society 62, 341 - 438. Rosen, D . E . , Forey, P . L . , Gardiner, B . C . & Patterson, C. 1981 . Lungfishes, tetrapods, pale ontology and plesiomorphy. Bulletin of the American Museum of Natural History 167, 163-275 .

1.9 Flight

1 . 9 . 1 Arthropods R . J . W O OTTON

Introduction Although mites and small spiders are frequently carried passively by air currents, insects are the only arthropods to have developed the power of active flight . Flight had already evolved by the early Namurian, when insects first appear in the fossil record . Namurian insects are rare, but Westphalian deposits - in particular the spectacular beds of Mazon Creek, Illinois (Westphalian C - D) (Section 3 . 1 1 . 5) - display large, developed faunas of winged insects, diverse enough to indicate that flight may have arisen by the end of the Devonian . A handful of primitively wingless (apterygote) Carboniferous insects are known; but there are no convincing 'protopterygotes' to indicate the nature of the transition - leaving ample scope for speculation . Debate has focused on two areas : the homology, nature, and functions of wing precursors; and the circumstances and means by which flight arose .

The homology and functions of the pro-wings Two hypotheses, both with their roots in the 19th century, are still in contention :

1 The paranotal lobe theory maintains that wings arose by enlargement of the second and third tho­ racic pairs of a segmental series of fixed, flat dorso­ lateral outgrowths, the paranotal lobes . Supporting

evidence is provided by the presence of such lobes on the first thoracic segment and sometimes the abdominal segments of adult Palaeozoic insects in several orders (Fig . lA), of a few later and extant forms, and of several Carboniferous nymphs in which the wing pads appear as part of a continuous series of lateral lobes on thorax and abdomen (Fig . 18) . This was the orthodox view until the late nineteen-seventies and is still widely supported, sometimes in a modified form (Rasnitsyn 198 1 ; Quartau 1986) .

2 The tracheal gill theory, revived by Wigglesworth (1976) and developed by Kukalova-Peck (1978, 1983), claims that wings are homologous with the abdomi­ nal gills of juvenile mayflies (Ephemeroptera), and that both are ultimately derived from articulated projections of ancient basal leg segments, now incorporated into the sides of the body . Kukalova­ Peck has quoted considerable supporting evi­ dence from fossil and extant insects, including Carboniferous and Permian mayfly nymphs with strikingly wing-like gills (Fig . 1C) . The theory, though by no means universally accepted, has now to be taken seriously . There is an important distinction between the two hypotheses. In the paranotal theory the lobes are presumed to have been immovable, and only later to have developed a mobile articulation with the thorax, as flapping flight evolved . In the tracheal gill theory the wing precursors are seen from the first as actively movable appendages whose form, articulation, and musculature altered progressively with their functions . Movable or not, the fore­ runners of wings would not have begun to generate useful aerodynamic forces until they had reached a certain size and shape, and it is necessary to find

1 . 9 Flight

73

1 A, Stenodictya (Order Palaeodictyoptera), reconstruction based on several species. Body (minus cerci and mouthparts) c. 60- 70 mm long. (After Kukalova 1970 . ) B, Rochdalia parkeri (Order Palaeodictyoptera), nymph. Upper Carboniferous . Length (excluding cerci) 22 mm. (After Wootton 1972 . ) C, Kukalova americana (Order Ephemeroptera), nymph . Lower Perrnian, Oklahoma . Length 21 mm. (Reconstruction after Hubbard & Kukalova-Peck 1980 . ) D , Balsa model, as tested by Wootton and ElIington (1991). Lengths 80 mm and 160 mm. The wingIets could be twisted around their mounting to alter the angles of attack. Fig.

some earlier functions to account for their reaching this stage . Fixed lateral lobes - most of them certainly not homologous with wings - occur in many modern insects, particularly in juveniles . They act variously: to streamline sedentary aquatic insects pressed to a substrate; and in several kinds of defence - in mimetic camouflage, as armament, or to obscure outlines or reduce shadows . All these have been suggested as possible pro-wing functions. A recent candidate is thermoregulation. Kingsolver and Koehl (1985), experimenting with model insects of three sizes equipped with several sizes of thoracic winglets, found that the latter increased heat uptake - up to a certain size beyond which no further effect could be detected . This size cor­ responded well with that at which aerodynamic

effects became detectable in wind tunnel experi­ ments . In the authors' view pro-wings developed as thermoregulatory structures, and were so pre­ adapted for flight. The functions proposed for the forerunners of wings in the tracheal gill hypothesis are more straightforward . The basal segments of the legs of modern apterygote insects bear articulated styles, homologous with neither gills nor wings but similar in form to those envisaged as early wing precursors . Their function is sensory . The flattened plate-like gills of many mayfly nymphs serve in gaseous ex­ change and can usually be flapped, increasing the rate of water flow over the body and providing ventilation, and in some cases propulsion . Gills are aquatic adaptations, whereas wings func­ tion in air. All variants of the tracheal gill theory

74

1 Major Events in the History of Life

assume that the ancestors of winged insects were aquatic or semiaquatic, at least as juveniles, and that the gills persisted in forms which became ter­ restrial, at least as adults . Rather inconveniently for this theory, extant apterygotes are predominantly terrestrial; but there is no reason why protoptery­ gotes should not have evolved by way of a second­ arily aquatic line . The adoption, or readoption of terrestrial habits then needs to be explained . Wigglesworth ( 1976) and Kukalova-Peck (1983) pro­ posed that aquatic or semiaquatic protopterygotes took to climbing up emergent or waterside veg­ etation, perhaps to feed on the energy-rich sporangia, and so became available for aerial dispersal .

The development of flight The many theories which have been put forward on the circumstances of the origin of flight fall into three groups . Variants of each were current when the paranotal lobe theory held exclusive sway, but some recent versions take account of the new factor of pro-wing mobility inherent in the tracheal gill hypothesis :

1 The running/jumping theory. Protopterygote in­ sects gained the speed necessary for flight by run­ ning or jumping into the air, perhaps to escape from predators, and planed or flapped to a landing.

2 The floating theory. Flight evolved in insects small enough to be carried up by winds or thermals . Pro­ wing enlargement was favoured by selection for high surface/volume ratio, and thus high drag .

3 The parachuting/gliding theories. Arboreal insects falling or jumping from a height used their pro­ wings initially for parachuting, then progressively for gliding and powered flight. In each hypothesis it is assumed that selection for improved aerodynamic efficiency led to the enlarge­ ment of the pro-wings on the second and third thoracic segments, and to the reduction and event­ ual loss of the remainder; and that performance was further enhanced by the development or improve­ ment of the power of flapping, with its associated morphological and physiological adaptations . One theory can be ruled out. Running and planing over level ground would be pointless, since even if take-off speed were reached the insect would begin to slow down as soon as it left the ground . Choice

between jumping, floating and paragliding is a matter of estimating relative probabilities . The hypotheses are not entirely mutually exclusive an insect jumping from an eminence into rising air would have features of all three - but their implications are rather different. The jumping theory requires that a protopterygote with a small pro-wing area could generate enough lift, with or without flapping, to achieve useful, stable, shallow flight, within the speed range which could be reached in a leap . The floating theory implies that an insect small enough to be carried by air currents would develop the morphological characteristics appropriate to powered flight . The parachuting/gliding theories require that pro-wings should initially maintain the insect in a stable attitude which would enable it to generate some lift in falling, and so glide or fly to a lower level slowly enough to avoid being damaged in landing . Several of these criteria have been investigated by Wootton and Ellington ( 1991), by dropping appropriately scaled cylindrical balsa models with serial winglets which could be rotated to particular angles relative to the body axis (Fig . 10), so testing the effects of one aspect of pro-wing mobility. They found that models scaled to be dynamically similar to an insect c. 25 mm long parachuted stably and relatively slowly at steep glide angles, if the winglets were rotated backward so as to be fully stalled at angles of attack around 85°, but were incapable of shallow glides . However, larger models corre­ sponding to insects c. 70 mm long - well within the size range of Palaeozoic forms - were capable of fast shallow glides, the speed and angle of which could be adjusted by minor changes in the angle of attack of the winglets . Removal of 'abdominal' winglets destroyed stability in the pitching plane, but this was readily restored by adding slender tail filaments, such as are found in many primitive winged insects (Fig. lA) . These results appear t o favour the parachuting/ gliding hypothesis, since shallow glides only proved possible at speeds well in excess of those normally achieved in a jumping take-off; a period of acceler­ ation in free fall is needed . The evidence also indi­ cates that the ability to change the angle of attack of the pro-wings would have been valuable in con­ trolling glide angle and speed, and perhaps in ensuring stalled soft landings . Preliminary unpub­ lished calculations suggest that flapping would have had negligible effect on flight performance in the

75

1 . 9 Flight early stages of flight evolution, but would have become increasingly effective as the pro-wings enlarged in association with improved gliding . The evolution of powered flight from passive floating is far harder to envisage . Selection for drift­ ing efficiency might favour the enlargement of body appendages, but with a high-drag morphology which would not adapt them for active flight . Selec­ tion would, however, favour small size, which would necessitate uncomfortably high flapping fre­ quencies even when the wings had become fully developed . The advantages of flapping at the pro­ wing stage would be infinitesimal .

Conclusion Recent discoveries notwithstanding, hard infor­ mation on the origin of insect flight is still rather scarce . On balance, the combined evidence from palaeontology, comparative morphology and experi­ mental biomechanics suggests that flight probably evolved in the Devonian, in medium to large arboreal insects initially bearing serial lateral ap­ pendages which may have been capable of being actively twisted, and perhaps flapped. The append­ ages may at first have served to stabilize and slow the insects' falls, but came to provide lifting sur­ faces, allowing shallow fast glides . There followed enlargement of the winglets closest to the centre of mass, to a size where flapping became effective in generating thrust and weight-support; and re­ duction of the remaining winglets, accompanied by enlargement of caudal appendages to prevent loss of stability . Though in no way proven, a scenario of this kind is both feasible and fairly parsimonious . No evo­ lutionary 'quantum leaps' would be required . Given the initial presence of small articulated lateral appendages, the insects could pass from wingless­ ness to active flight by gradual stages, all of which make functional sense .

References Hubbard, M.D. & Kukalova-Peck J . 1980 . Permian mayfly nymphs: new taxa and systematic characters. In : J . F . Flannagan & J . E . Marshall (eds) Advances in Ephemeroptera biology. Plenum Publishing Corporation, New York. Kingsolver, J . G . & Koehl, M.A.R. 1985. Aerodynamics, thermoregulation, and the evolution of insect wings : dif­ ferential scaling and evolutionary change . Evolution 39, 488 -504 . Kukalova, J. 1970 . Revisional study of the Order Palaeo­ dictyoptera in the Upper Carboniferous of Commentry,

France . Psyche, Cambridge 77, 1 -44. Kukalova-Peck, J. 1978. Origin and evolution of insect wings and their relation to metamorphosis as documented by the fossil record. Journal of Morphology 156, 53- 126. Kukalova-Peck, J . 1983. Origin of the insect wing and wing articulation from the arthropod leg . Canadian Journal of Zoology 61, 1618- 1669 . Quartau, rA. 1986. An overview of the paranotal theory on the origin of insect wings . Publicar;oes do Instituto de Zoologia 'Dr Augusto Nobre' Faculdade de Ciencias do Porto 194, 1 -42. Rasnitsyn, A.P. 1981 . A modified paranotal theory of insect wing origin. Journal of Morphology 168, 331 -338 . Wigglesworth, V.B. 1976. The evolution of insect flight. In : R.C. Rainey (ed . ) Insect flight. Symposium of the Royal Entomological Society of London No . 7, pp . 255- 266. Blackwell Scientific Publications, Oxford. Wootton, R.J. 1972 . Nymphs of Palaeodictyoptera (Insecta) from the Westphalian of England . Palaeontology 15, 662 - 675 . Wootton, R.J. & Ellington, c.P. 1991 . Biomechanics and the origin of insect flight. In: J.M.V. Rayner & R.J. Wootton (eds) Biomechanics and Evolution . Society for Experimental Biology, Seminar Series. Cambridge University Press, Cambridge.

1 . 9 . 2 Vertebrates K . PADIAN

Introduction Three groups of terrestrial vertebrates have evolved flight independently : pterosaurs (Late Triassic ­ Late Cretaceous), birds (Late Jurassic -Recent), and bats (Eocene - Recent) . By 'flight' is meant flapping flight; parachuting, gliding, and soaring are other, different modes of flight . Parachuting is descent slowed mainly by drag; in gliding, lift predominates and the angle of descent tends not to exceed 45° . Soaring, as opposed to these two passive modes of flight, actively uses the energy of rising therrnals and air currents to maintain height, even though the wings are fixed . Soaring habits seem to have evolved only in active flyers, not in passive ones, although aerodynamically there seems to be no reason why passive flyers could not soar; however, their wings are not long and narrow like those of other soarers .

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1 Major Events in the History of Life

Three principal factors are important in under­ standing the origin of flight and its evolutionary history in each flying group :

1 Aerodynamic considerations define the physical requirements for flight and restrict the morphologi­ cal and ecological possibilities for animals that fly . Aerodynamics of living vertebrates are well enough known to shed considerable light on parameters for fossil forms (Rayner in Hecht et al. 1985; Rayner 1988) . Most important is the generation of sufficient thrust to create a vortex wake that propels the animal forward . Wing design, planform, and muscle physiology are instrumental in quantifying flight capabilities, and can to some extent be modelled in fos sil forms by comparison with living ones.

2 Functional considerations are important in under­

standing the evolution of the flight apparatus and the generation of the flight stroke, the latter being the single property that defines powered flight (Padian 1985) . All three groups of flying vertebrates use a vertical or down-and-forward stroke of the forelimbs to generate thrust . Each group, although built on the general tetrapod plan, has modified its basic equipment in different ways (Fig . 1 ) . For example, the wing is functionally divided into three segments, of which the outermost is principally supported by the fourth finger in pterosaurs, the wrist and fused fingers in birds, and the unfused fingers in bats . But despite differences in the equip­ ment, the flight strokes are essentially the same . 3

The evolution of flight is also influenced by phylo­ genetic factors . Organisms have to use what they inherit in order to solve evolutionary and ecological problems; their past history dictates in large measure what they are capable of doing in future . Therefore, understanding the phylogeny of organ­ isms in detail helps us to understand the ecological milieu from which they evolved. As a result, com­ plex adaptations may be dissected part by part simply by assembling the evolutionary sequence of forms that evolved the adaptation . Of course, this must be done by reference to other, functionally independent character sets (Gauthier & Padian in Hecht et al. 1985; Padian 1987) . In studying the evolution of flight, then, the aero­ dynamic factor provides us, in effect, with the laws that bound the possible solutions to the problem . The functional factor shows how the problem is solved. The phylogenetic factor shows much about why a given animal solved the problem in the particular way it did . With these three approaches in mind, the evolutionary histories of flight in pterosaurs, birds, and bats may be considered .

Pterosaurs These first flying vertebrates were archosaurs very closely related to dinosaurs, and the common ances­ tor of the two groups seems to have been a small, lightly built, bipedal form of the Middle Triassic . Typically, pterosaurs have been pictured as bat-like lizards with poor terrestrial capability, but a large suite of features suggests that they were instead agile bipeds that moved much more like birds and other dinosaurs (Padian 1985) . The wings were nar­ row and could not have been attached to the legs without spoiling vortex patterns over the wing. Pterosaurs have been divided historically into two groups : the earlier, paraphyletic 'Rhamphorhyn­ choidea' and the later, monophyletic Pterodactyl­ oidea (Wellnhofer 1978) . The 'rhamphorhynchoids' retained the long tail of their archosaurian ancestors, hyperelongated the metacarpus and (especially) the fourth finger for flight, and stretched a wing of skin behind the forelimb running along the body wall to the tail . The wing membrane was invested with countless stiffening 'fibres', which were intercalated and oriented through the wing like the feather shafts of birds or the fingers of bats (Padian 1985) . 'Rhamphorhynchoids' also hyperelongated the two phalanges of the fifth toe; adaptations for grasping or perching have been suggested without close argument, but the elongation was equally likely to have been merely a developmental conse­ quence of elongating the outer digit of the hand . It is often observed that in the history of any flying animals (including humans), early designs are highly stable aerodynamically . In more advanced forms, on the other hand, the designs become inherently unstable as the neurological control sys­ tems become more sophisticated. Pterodactyloid pterosaurs, like post-Archaeopteryx birds, lost the tail, a primary mechanism of dynamic stability . Pterodactyloids also shortened the humerus (the first functional segment of the wing), lengthened the metacarpus (much of the second section), and tended to shorten the wingfinger slightly (the third section) . Aerodynamic reasons for this are not yet understood, but stability was probably involved . Large size and soaring habits characterized several lineages within Pterodactyloidea, including those of Pteranodon and Quetzalcoatlus (Late Cretaceous, North America), and these represented most of the latest known forms in the fossil record . No known pterosaurs show particular arboreal specializations, but it must be remembered that the terrestrial fossil record is biased toward aquatic environments and against forest and upland habitats .

1 . 9 Flight

77

cor

fu rc

s

te r

ster bat

pterosa u r

bird

c

bird

11

I-I l l

hum

pterosau r

hum

bat

v ca Fig. 1 Diagrammatic comparisons of the thoracic regions and forelimbs of the three groups of vertebrate flyers. Thoracic regions (above) are seen from the front; left forelimbs (below) in ventral view. Structurally, the coracoids of pterosaurs and birds seem to be functionally analogous to the clavicles of bats, as do the furcula of birds, the cristospine of pterosaurs, and the manubrium of bats . Abbreviations : e, carpus; ca, calcar; clav, clavicle; cor, coracoid; Jure, furcula; hum, humerus; mc, metacarpus; pt, pteroid; r, radius; se, scapula; ster, sternum; u, ulna; [- V, numbered digits. Not to scale . (From Padian 1985 . )

78

1 Major Events in the History of Life

Birds

Archaeopteryx, from the Late Jurassic Solnhofen Limestone of Bavaria (Section 3 . 1 1 . 7) is the first known bird, recognized by its flight feathers . In the nineteen-seventies J . H . Ostrom established its ancestry from among small carnivorous (coelu­ rosaurian) dinosaurs, an idea first advanced a century ago by T . H . Huxley . Gauthier (1986) used over 200 nested synapomorphies to document the sequence of acquisition of characters that not only show how the major archosaurian groups are related to each other, but also how those characters relevant to flight evolved . Some features considered typically 'avian' , such as the furcula (fused clavicles) and calcified sterna, appeared in carnivorous dinosaurs at a more general level than Aves. Other features, such as the perching foot, the reduced tail and teeth, and the fused carpometacarpus, ap­ peared well after Archaeopteryx. Little is known of Cretaceous birds apart from a few open-water fo�ms . The loon-like Hesperornis and the tern-like Ichthyornis (Late Cretaceous, Western Interior, North America) are not members of the orders of living birds; most of these have their first records in the Eocene or later . The refinement of flight adap­ tations in avian evolution is poorly known and must be reconstructed mainly with reference to living forms . Recent discoveries of Early Cretaceous birds from Spain show that by that time the dorsal vertebrae were reducing in number, the tail had been shortened to a pygostyle, the coracoids were strut-like and braced to the sternum, and the furcula (wishbone) had a prominent hypocleidium . A perching foot with trenchant recurved claws appears to have been well developed . Archaeopteryx is perhaps the world' s most famous fossil; it is the basis for a great diversity of ap­ proaches and viewpoints on the origin of birds and the early evolution of their flight (Hecht et al. 1985) . The traditionally favoured view is that birds evolved in trees and passed through a fully gliding stage on the way to active flight (Bock in Hecht et al . 1985) . It is easiest to evolve flight in this way (Rayner; Norberg; in Hecht et al. 1985), but this does not exclude other possibilities . The view that flight evolved from a small terrestrial animal that ran and leaped into the air, gaining flight gradually by the elaboration of 'pro to-wings, ' has recently been ad­ vocated (Ostrom; Gauthier & Padian; Caple et al .; in Hecht et al. 1985) . The advantage of this view is that it is rooted in the evolution and ecology of avian ancestors, whereas the 'arboreal' theory is not; but

the disadvantage is the relative difficulty of evolving flight 'from the ground up' . Terrestrial speeds needed for take-off are uncomfortably high, judging from small living bipeds (Rayner in Hecht et al. 1985), whereas speed is easily gained by dropping out of a tree. It is difficult to see what evidence could resolve this question; most likely, some com­ promise between the two extremes will be most fruitful .

Bats Little is known about the early evolution of bats; like pterosaurs, when they first appear in the fossil record (the Eocene Icaronycteris: Jepsen 1970) they are fully formed flyers, and the evolution of their flight can only be reconstructed from the skeletons of the earliest forms . Like gliding mammals, and un­ like birds and pterosaurs, bats incorporate the hind­ limbs in the wing membrane, which explains why their terrestrial ability is so poor: their fore- and hind limb locomotory systems are not independent, and stress has clearly been placed on the forelimb system. In all respects, bats seem to have followed the model for evolution from gliding forms (Rayner; Norberg; in Hecht et al. 1985) . Based on analyses of the general distribution of their characters, bats appear to have evolved from a group of generally nocturnal, arboreal, insectivorous - omnivorous placentals . Some facility for echolocation and hang­ ing upside down would seem to have appeared at an early stage in bat evolution . A nocturnal, arboreal form that could glide and hang upside down (thus freeing its forelimbs from most locomotory func­ tions) would be a reasonable ancestor (Padian 1987) . For this reason, recent studies of the phylogenetic position of Chiroptera have generated considerable excitement and controversy . Although several workers have claimed that the Chiroptera are diphyletic (separate origins of megabats and microbats), cladistic studies by Novacek and his colleagues (e . g . Wible & Novacek 1988) have pro­ vided a consilience of skeletal and molecular evidence that appears to support chiropteran monophyly . Moreover, a suite of cranial and post­ cranial characters suggests that the closest sister­ taxon to Chiroptera is Dermoptera, the so-called 'flying lemurs' now restricted to Southeast Asia . If Novacek and his co-workers are correct, some habits of the living dermopteran Cynocephalus, coincident with those discussed in the preceding paragraph, may shed light on the ecology of the common ancestor of the two groups.

1.10

Angiosp erms

References Gauthier, J.A. 1986 . Saurischian monophyly and the origin of birds . In: K. Padian (ed . ) The origin of birds and the evolution of flight, Memoirs of the California Academy of Sciences, No. 8, pp . 1 -55. Hecht, M.K., Ostrom, J . H . , Viohl, G . & Wellnhofer, P. (eds) 1985 . The beginnings of birds . Proceedings of the First Inter­ national Archaeopteryx Conference, Eichstatt 1 984 . Freunde des JuraMuseums, Eichstatt, F.R.G. Jepsen, G . L . 1970. Bat origins and evolution. In : W.A. Wimsatt (ed . ) Biolo:.,'!} of bats, Voz. I. Academic Press, New York. Padian, K. 1985 . The origins and aerodynamics of flight in extinct vertebrates. Palaeontology 28, 41 3-433.

79

Padian, K. 1987. A comparative phylogenetic and functional approach to the origin of vertebrate flight. In: M . B . Fenton, P. Racey & J.M.V. Rayner (eds) Recent advances in the study of bats, pp. 3-22 . Cambridge University Press, New York. Rayner, J.M.V. 1985 . Vertebrate flight: a bibliography to 1 985. University of Bristol Press, Bristol. Rayner, J.M.V. 1988. The evolution of vertebrate flight. Biological Journal of the Linnean Society 34, 269 -287. Wellnhofer, P. 1978 . Handbuch der Palaeoherpetologie. Teil 14: Pterosauria. Gustav Fisher Verlag, Stuttgart. Wible, J.R. & Novacek M.J. 1988. Cranial evidence for the monophyletic origin of bats . American Museum Novitates 2911, 1 - 19 .

1.10 Angios p erms M . E . COLLINSON

Introduction The angiosperms or flowering plants are the most diverse living plant group with over 250 000 species . They dominate world vegetation, with the exception of moss-lichen tundra and high latitude northern hemisphere coniferous forest. They exhibit a wide range of life form and strategy, ranging from tiny free-floating aquatic duckweeds through epiphytes and lianas to tall forest trees . This diversity and dominance has, however, been attained relatively recently in terms of Earth history, apparently within the last 120 million years . The origin and subsequent diversification of the flowering plants has influ­ enced community structure and the evolution of all other biotas .

Early fossil evidence Several synapomorphies of the angiosperms (Crane 1985; Doyle & Donoghue in Friis et al . 1987) are features of reproductive biology not amenable to recognition in the fossil record . Characteristic pol­ len, wood, and leaves (Fig . 1) may, however, be easily detected . Like other plants, angiosperms are largely represented in the fossil record by organs (like pollen, leaves, seeds) which are dispersed or shed during life . The smallest and most widely

dispersed are most likely to be preserved . It is to be expected, then, that the earliest recognizable angio­ sperm fossils are pollen grains with the tectate/ columellate wall (Fig . 1G) . These mono sulcate pol­ len, named Clavatipollenites (Fig. 2B), occur in the Early Cretaceous (Barremian) of England, West Africa, Argentina, and eastern North America (Muller; Walker & Walker; in Dilcher & Crepet 1985) . Clavatipollenites pollen are very similar to grains produced by modern members of the magnoliid dicotyledon family Chloranthaceae, e . g . Ascarina (Walker & Walker in Dilcher & Crepet 1985) . As pollen of other magnoliid plants lack the diagnostic wall structure and plant organs may evolve at different rates, there is no reason to assume that Clavatipollenites pollen represent either the earliest or the most primitive flowering plants.

Cladistic analyses Recent cladistic analyses of fossil and modern seed­ plant groups (Crane 1985; Doyle & Donoghue 1986; Doyle & Donoghue in Friis et al . 1987) imply a pre­ Cretaceous origin of angiosperms, possibly as early as the Triassic . In these analyses an anthophyte clade can be defined (Fig . 3B), for which the sister group may be one of several Mesozoic seed plants

1 Major Events in the History of Life

80

,+�

en c C c o

G

.. . . ::. :: '

-:<)!",

:':0: : :

.' . a: .

B

Fig. 1 Characteristic features of angiosperms detectable in the fossil record . A-C, vessel elements (lengths vary from about 200 - 1 000 Ilm) . D, E, dicotyledon leaf (length about 5 cm) with venation detail. F, tricolpate pollen grain (diameter about 30 Ilm) . G, section of pollen wall (thickness about 1 - 3 Ilm) showing endexine (en) and ectexine (ec) divisible into footlayer (f), columnar layer (c), and tectum (t) . (From Friis et al . 1987.)

A

Fig. 2 A, Time of appearance of major floral types. Solid lines based on flower fossils, dashed lines on indirect evidence - mostly pollen . (From Friis & Crepet ill Friis et al. 1987.) B, Clavatipol/ellites, monosulcate pollen (length 20 Ilm) . (From Stewart 1983 . )

B

(Caytonia, glossopterids, corystosperms) that exhibit varying degrees of ovule protection, net leaf ve­ nation, fused pollen sacs, etc . (all later elaborated upon in members of the anthophyte clade) . Flower­ like organization of reproductive structures (Fig. 3A) typifies members of the clade, hence the pro­ posed term anthophyte . This feature can no longer be seen as a uniquely angiosperm attribute . Fig . 3A represents the inferred character transformations in the reproductive structures of members of this clade . In angiosperms the microsporophyll ( stamen) is reduced but the megasporophyll ( carpel) remains complex . In Bennettitales the megasporophyll is reduced to a uniovulate unit but the microsporophyll remains complex . In Gnetales both micro- and megasporophyll are reduced. =

=

According to these cladistic analyses the Gnetales are the closest living relatives of the angiosperms and these two groups share a common ancestry (along with Bennettitales and Pentoxylon) amongst Mesozoic seed plants . Careful study of these, es­ pecially Triassic representatives, and a clearer understanding of the fossil record of Gnetales, will clarify the phylogenetic history of the anthophyte clade .

Early radiation Following

the

widespread

appearance

of

Clavatipollenites pollen during the Barremian, other angiosperm pollen types occur in later Barremian and Aptian strata . These include probable

1.10

3 A, Major character transformations in reproductive structures inferred from Fig. 3B and present in : (a) hypothetical ancestor; (b) angiosperm : (c) Bennettitales; (d) Gnetales. (From Friis et al. 1987.) B, The anthophyte clade: Ag angiosperms, Bn Bennettitales, Pn Pentoxylon, Gn Gnetales, s sister group involving one or more of corystosperms, glossopterids or Caytonia according to author. (After Doyle & Donoghue in Friis et al.

Angiosp erms

81

Fig.

=

\

=

=

=

=

A

1987.)

Chloranthaceae; forms similar to those of modern monocotyledons; and forms referable to the Winteraceae, another family of the magnoliid dicots . In the Aptian, tricolpate pollen (Fig . IF) first indicate the presence of non-magnoliid ('higher') dicoty­ ledons (Hamamelidae or Ranunculidae) . In the Albian, pollen with endoapertures (tricolporate) signal the occurrence of probable Dilleniidae or Rosidae . Angiosperm pollen accounted for only up to 1% of palynofloras in the Barremian . By the late Albian they accounted for up to 70% in some low palaeolatitude areas, with lower proportions in middle palaeolatitudes . In the Turonian, angio­ sperms dominated palynofloras from many areas of the world (Muller; Walker & Walker; both in Dilcher & Crepet 1985) . Details of the early phase of angiosperm leaf diversification are largely based on material from eastern North America . Angiosperm leaves may be characterized by reticulate venation, in a hierarchi­ cal system often with free ending veinlets (Fig . ID, E) . Most Aptian angiosperm leaves are small, entire­ margined and simple with pinnate venation, some­ times with a poorly developed hierarchy . Middle to Late Albian assemblages show an increase in diver­ sity of leaf form, including pinnatifid and palmately lobed forms and cordate leaves . Forms similar to those of modern magnoliid (Chloranthaceae), hamamelid (Platanaceae), and rosid dicotyledons are recorded from the Albian (Upchurch in Dilcher & Crepet 1985; Upchurch & Wolfe in Friis et al . 1987) . A statistical assessment of the proportion of dif­ ferent plant groups in leaf floras (see Fig . 5) clearly

/ ( a)

demonstrates the rapidity with which angiosperms became dominant elements, replacing cycadophytes and pteridophytes during the Early and earliest Late Cretaceous . The replacement generally took place later at higher palaeolatitudes. Angiosperm floral provinciality was well established by the Late Cretaceous . Angiosperm herbs and small woody plants first entered early successional habitats such as stream sides, coastal plains, and other disturbed areas in a similar manner to the weeds of today (Retallack & Dilcher 1986; Crane in Friis et al. 1987) . During the Late Albian they diversified into full aquatics, forest understory shrubs and riparian trees . Early in the Late Cretaceous angiosperms (probable shrubs and small trees) remained effective colonizers and ex­ panded first into environments previously domi­ nated by cycadophytes (including Bennettitales) and ferns . The rise of angiosperms may have influenced certain dinosaur feeding strategies, reflected in the Late Cretaceous radiation of ornithischian her­ bivores (Coe et al. in Friis et al. 1987) . Although angiosperms clearly dominated vegetation in many areas by the early Late Cretaceous, several signifi­ cant advances took places later (see below) .

Early floral biology Recently, data on fossil flowers and, more rarely, on partially reconstructed whole plants has added to that from dispersed pollen and leaves (Friis & Crepet; Crepet & Friis; in Friis et al. 1987) . Amongst the earliest known fossil flowers from the early

82

1 Major Events in the History of Life

Late Albian of eastern North America are forms (Fig. 2A(a)) which are very similar to modern members of the Chloranthaceae, e . g . Chloranthus . The floral morphology suggests insect pollination, as does their similarity to modern insect pollinated Chloranthus . In contrast, the abundance of the early Cretaceous pollen Clavatipollenites suggests wind pollination, as in modern Ascarina. In the same fossil flora unisexual platanoid flowers also occur (Fig . 2A(c)) . These small, platanoid and chloranthoid flowers are usually considered derived by comparison with large showy bisexual flowers which also occur in the Albian (Fig . 2A(b)) . The best known example is from the Albian/Cenomanian boundary of the Western Interior of North America (Fig . 4; Dilcher & Crane in Dilcher & Crepet 1985) . This plant has been reconstructed using organic connection, attachment scars, and association evidence, from a suite of fossil organs occurring in one thin sedi­ mentary unit . Its multifollicular fruit (named Archaeanthus) represents the primitive condition as predicted from, but not represented in, modern flowering plants . Other features of the flower (numerous free, spirally arranged parts) also con­ form to the traditional, hypothetical angiosperm archetype . However, certain a spects of the whole plant, e . g . the lobed leaf, are more advanced . The 'Archaeanthus plant' shares most features with members of the Magnoliales, amongst living plants, but it cannot be assigned to a modern family . Strata of the same age have also yielded a more derived flower form (Fig . 2A(d)) with parts in whorls of five . Clearly all of these floral forms (Fig . 2A(a - d)) were represented very early in the evolution of flowering plants . They confirm the pattern of rapid diversifi­ cation as inferred from pollen and leaves, and the early differentiation of 'higher' dicotyledons (Crane 1989) . They also suggest the early existence of wind pollination and a range of insect pollination strategies .

Pollination biology and dispersal strategy Insect pollination may characterize all members of the anthophyte clade and was therefore not a con­ trolling factor in angiosperm origins . The enclosing carpel (megasporophyll enclosing ovules) and the receptive stigmatic surface on the carpel are, how­ ever, unique to the angiosperms . Together these permit control of pollen germination, hence fertiliz­ ation, and allow for the exploitation of incompati­ bility mechanisms . Such mechanisms permit or

4 Reconstruction of one of the best known Cretaceous angiosperms, 'Archaeanthus' from the Dakota Formation, Albian/Cenomanian boundary, Kansas, U . 5 . A . External flower diameter about 130 mm. (From Dilcher & Crane in Dilcher & Crepet 1985 .) Fig.

enforce cross fertilization with resultant enhanced variation . The carpel also provided for new means of seed dispersal through a range of fruit structures . Combined, these features increase speciation rates and reduce extinction rates, resulting in increased diversity and potential dominance in vegetation. Such features can be best exploited through con­ trolled (biotic) transfer of pollen to the stigma rather than the more haphazard wind pollination . The late Cretaceous and Early Tertiary evolution of floral form (Fig . 2A) reveals the continued elabor­ ation associated with new pollination vectors . The earliest insect pollinated angiosperms probably possessed generalist flowers visited by a range of insects . Specialization for beetle pollination is indi­ cated by the large robust magnolialean flowers with prolific pollen production (Fig . 2A(b)) . Early Late Cretaceous flowers with reduction and fusion of whorled parts and nectar glands in discs (Fig . 2A(d - f)), along with inferior flowers with stout styles (stigmatic stalks) (Fig . 2A(g)), suggest increasing specialization for more specific insect pollinators, including those feeding on nectar as well as pollen. In the latest Cretaceous and Early

83

1 . 1 0 Angiosperms

Pte r i d o p hytes 75 %

50%

Cycadop hyte s

Angiosperms

25%

C o n i fers

5 Percentage contribution of major plant groups to ancient leaf floras from Jurassic to Palaeocene. (From Crane in Friis et al. 1987 . )

Fig.

Jur

Neo

Tertiary further elaborations such a s zygomorphy (bilateral not radial floral symmetry, Fig . 2A(h, j)), brush flowers (Fig. 2A(i)), and long corolla tubes (Fig. 2A(k)) were developed. These are associated with advanced pollinators like bees and butterflies . Some of the more specialized 'faithful' plant pol­ linator relationships were established by the Eocene (Crepet & Friis in Friis et al. 1987) . Fruiting structures also diversified to include fleshy fruits, along with a range of dry nuts and winged fruits (Tiffney in Dilcher & Crepet 1985; Friis & Crepet in Friis et al. 1987) . The fruits not only indicate a range of dispersal types but also a range of establishment strategies . Large seeds, able to establish in shaded, canopy covered forest, became more widespread in contrast to the smaller seeds of the earliest angiosperms . This is consistent with an early Tertiary origination of angiosperm-dominated forests with angiosperms as the tall canopy trees, inferred from the fossil record of leaves and wood (Crane; Upchurch & Wolfe; both in Friis et al. 1987) .

Later radiation The fossil records of pollen, leaves, fruits, seeds, flowers, and wood all point to a major radiation and modernization of flowering plants in the latest Cretaceous and Early Tertiary (Fig . 5) . This may in part have been in response to the Cretaceous/ Tertiary event, followed by the diversification of mammals replacing dinosaurs as the main large vertebrates on land (Section 2 . 1 3 . 7) . Extinction of the dinosaurs, whether gradual or sudden, resulted in the removal of large herbivores which were not

C retace o u s

Pa l

replaced by an equivalent diversity of large her­ bivorous mammals until the end of the Eocene (Coe et al. ; Collinson & Hooker; Wing & Tiffney: in Friis et al. 1987) . The later Tertiary saw a further radiation of angiosperms, particularly of the her­ baceous groups which represent much of their modem diversity . Grasslands, for example, probably originated in the latest Oligocene or Miocene, perhaps in response to grazing mammals (Section 1 . 1 1 ) . Plant communities reconstructed from Early Ter­ tiary floras are often said to be similar to those of the present day, although in reality none was iden­ tical in composition. Instead they combined el­ ements whose nearest living relatives are widely separated ecologically and geographically (Collinson & Scott 1987; Crane in Friis et al. 1987) . Some wetland herbaceous and wooded communities have a good fossil record which may eventually permit recon­ struction of their evolution . In other cases, e . g . grasslands and montane forests, the record i s far less promising. Future studies should emphasize the sediment­ ological and taphonomic context of angiosperm fossils . This, together with more critical comparative studies of fossils and their living relatives, will lead to a fuller understanding of angiosperm evolution .

References Collinson, M . E . & Scott, A.C. 1987. Factors controlling the organization and evolution of ancient plant communities. In: J . H.R. Gee & P.S. Giller (eds) Organization of communi­ ties: past and present, pp. 399-420 . Blackwell Scientific Publications, Oxford.

84

1 Major Events in the History of Life

Crane, P.R. 1985 . Phylogenetic analysis of seed plants and the origin of angiosperms. Annals of the Missouri Botanical Garden 72, 716-793 . Crane, P.R. 1989 . Palaeobotanical evidence on the early radiation of nonmagnoliid dicotyledons . Plant Systematics and Evolution 162, 165- 191 . Dilcher, D. & Crepet, W . L . (eds) 1985 . Historical perspectives of angiosperm evolution. Annals of the Missouri Botanical Garden 71 , 347- 630. Doyle, J.A. & Donoghue, M.J. 1986. Seed plant phylogeny

and the origin of angiosperms: an experimental cladistic approach. The Botanical Review 52, 321 -431 . Friis, E . M . , Chaloner, W.G. & Crane, P.R. (eds) 1987. The origins of angiosperms and their biological consequences. Cambridge University Press, Cambridge. Retallack, G.J. & Dilcher, D.L. 1986. Cretaceous angiosperm invasion of North America. Cretaceous Research 7, 227- 252.

Stewart, W.N. 1983 . Paleobotany and the evolution of plants. Cambridge University Press, Cambridge.

1 . 11 Grasslands and Grazers J . R . T H O M A S S O N & M . R . V O O RH I E S

Grasslands Modern grasslands cover more than 30% of the Earth's land surface and contain more than 10 000 species of grasses that provide more than half the calories consumed by animals (including humans) every day. Yet, in spite of their obvious importance, the origin and evolution of grasslands has remained relatively obscure until recent decades when evi­ dence from fossil grasses, vertebrates, and soils (palaeosols) has increased significantly. A review by Thomasson (1987) of the history of palaeoagraostology indicates that undoubted fos­ sil grasses are more widespread in the fossil record than previously thought, having been reported from most continents and many stratigraphic levels dating from the Oligocene; reports of probable fossil grasses may extend the age of the oldest grasses to the Eocene . The macromorphological remains of undoubted fossil grasses include anthoecia (husks) and caryopses, leaves, stems, roots, and rhizomes; many show external and internal micromorphologi­ cal details (Fig. 1) that provide extensive information about phylogenetic relationships in several groups of grasses, the physiological pathways of photosyn­ thesis in certain grasses, and diet in some her­ bivores . Macrofossils also ultimately constitute the most direct evidence for understanding the origin and evolution of grasslands . Microfossils, in the form of pollen and silica bodies (phytoliths), gene­ rally are less reliable for documenting the origin and spread of grasses and grasslands .

The most complete and remarkable record o f fossil grasses comes from Late Oligocene - Miocene strata in central North America (Thomasson 1987) . By the Late Miocene, all subfamilies of the Gramineae are present in these deposits (along with abundant remains of grazers), clearly indicating the wide­ spread presence of grasslands in that region since at least the Middle Miocene . The spread of grasslands in central North America during the Tertiary is evidenced by a dramatic in­ crease in both numbers and varieties of fossil grasses (Thomasson 1987) . From a compara­ tively limited Late Oligocene record of one genus (Berriochloa, including Stipidium) with only two or three species, a rich Late Miocene record comprises at least six genera (Archaeoleersia, Berriochloa, Graminophyllum, Nassella, Paleoeriocoma, and Panicum) with as many as 20 - 30 different species . Although living descendants o f these Late Miocene grasses (e . g . Nassella and Piptochaetium) are es­ pecially common in open grasslands of Central and South America, some are found throughout the world (e .g. Panicum and Stipa) . Tertiary grasslands undoubtedly disappeared under the harsh climate of the Pleistocene and were replaced by boreal forests and taiga; consequently modern grasslands are a post-Pleistocene development in central North America . Fossil evidence for grasslands in other parts of the world is limited . Palmer (1976) provided con­ clusive evidence from grass cuticles for the presence

85

1 . 1 1 Grasslands and Grazers

A, Cross-section of vascular bundle in a grass leaf from Minium Quarry, Late Miocene, Northwest Kansas, x 500. Note the double bundle sheaths. M mestome, P outer parenchyma, V metaxylem vessel elements, and C slightly radiate chlorenchyma. B, Surface of a grass leaf from locality K045 in the Late Miocene Lukeino Formation, Kenya, x 620 . L long cells with sinuous walls, S stomata, and B silica body cavities. (Photograph A by J. R. Thomasson, B by B. Jacobs.) Fig. l

=

=

=

=

=

=

=

of open grasslands during the late Pleistocene in Africa; and B . Jacobs and G . J . Retallack indepen­ dently (personal communication) have recently dis­ covered fossil grasses in Miocene strata in Kenya that show great potential for elucidating the role of grasses during the Late Tertiary in Africa (Fig . lE). Although well preserved grasses are known from Europe, they have not been studied sufficiently to suggest a specific habitat (e . g . grassland, woodland, etc . ) . Next to fossil grasses themselves, the strongest indirect evidence for the origin and evolution of grasslands comes from studies of the dentition and skeletal structure of fossil vertebrates . Some studies of the vertebrate evidence suggest that grasslands first appeared in South America during the Eocene or Oligocene, in Africa during the Oligocene, in North America during the Late Eocene to Early Oligocene, in Central Asia, China, and Western Asia during the Miocene, and in Australia during the Pliocene (Webb 1977; Wright 1986) . Other stud­ ies (see below) of large, mobile herbivores such as horses suggest that true grasslands (i . e . savannas, as opposed to woodlands with patches of grass) did not appear until the Middle Miocene . Finally, palaeosols (fossil soils) provide clues to the emergence of grasslands . Fossil grassland soils can be recognized by the presence of calcic horizons, phytoliths (silica bodies), and grass-like root traces (the biological nature of the latter has only oc­ casionally been documented by cellular details) .

Palaeosols provide evidence for many features of ancient environments, including the nature of the plant community (i . e . grassland vs . forest) (Wright 1986) . Contrary to most vertebrate evidence, palaeo­ sols suggest that grasslands of a savanna or pampas type may have appeared during the Oligocene in North and South America; that small areas of rela­ tively treeless prairie may have emerged in cen­ tral North America (South Dakota) by the Late Oligocene; and that grasslands may have appeared in Northern Pakistan and India, and the Rift Valley in Kenya and Tanzania during the Miocene .

Grazers One of the most striking features of the later Cenozoic (Neogene) terrestrial fossil record on all continents is the appearance of hooved mammals with limbs adapted for high speed running and dentitions adapted for dealing with a diet high in cellulose and/or grit. In the modern world these adaptations occur in such herbivorous animals as horses, bison, and certain antelopes and kangaroos that inhabit open grasslands and subsist exclusively or primarily on a diet of grasses . These 'grazers' contrast with the 'browsers' (e . g . moose, tapir) that consume primarily the leaves of dicotyledonous plants . Modern ecological studies have shown that many herbivores both graze and browse and are thus 'mixed feeders', but the end members are

86

1 Major Events in the History of Life

none the less sufficiently distinct to be useful cat­ egories in discussing the evolution of the ungulates, or hooved mammals . Structural features of the limbs and dentitions that distinguish modern grazers from browsers have been used to separate fossil ungulates into feeding categories, and to document the fact that the grazing habit has arisen independently in many families, primarily during and since the Miocene (a time of world-wide climatic deterioration; Janis 1984) . Most published studies have identified as grazers those ungulates with hypsodont teeth (high crowned, where the height of the enamel-covered crown ex­ ceeds its length or width) . Complex infoldings of the tooth crown and the presence of reinforcing cement on the occlusal surface are additional fea­ tures characterizing the hypsodont teeth of nearly all living grazers . The postcranial skeletons of fossil ungulates with hypsodont teeth, where known, usually exhibit elongate limbs, especially in the distal segments (below the wrists and ankles) . The correlation between grazing habit and hypsodont teeth and long limbs is good, but not perfect; an exception is the hippo, which does not have ex­ ceptionally high-crowned teeth and certainly lacks long limbs, but is clearly a grazer in the strictest sense, consuming only grass . (Would-be palaeo­ ecologists can perhaps take some small comfort from the fact that the hippo feeds only on tender new growth - in contrast to the zebra, a more orthodox grazer, which consumes the older, tougher tops of plants) . With these qualifications in mind the most fre­ quently cited example of a progressive adaptation to grazing - the evolution of the horse - may be examined . The accepted dogma among vertebrate palaeontologists has been that extensive grasslands appeared in the Miocene simultaneously with the first horses having high-crowned teeth and reduced lateral digits ('side toes') on the feet. Since it was first stated in the nineteenth century by R. Kowalevsky, the hypothesis of a coevolutionary relationship between the spread of siliceous grasses and the diversification of the horse family has re­ ceived support from an increasingly well docu­ mented fossil record of the Equidae, especially in North America . In the Eocene and Oligocene all horses had rela­ tively short, strongly tridactyl feet and very low­ crowned teeth, although a trend toward increased lophodonty ('ridginess') of the tooth crowns can be observed in the transition from Early Eocene Hyracotherium through Late Oligocene Miohippus.

Recent study of microwear facets on the cheek teeth show that these early horses ate relatively soft, low­ fibre vegetation that required crushing and a limited amount of slicing, but little or no grinding (Rensberger et al. 1984) . This interpretation is con­ sistent with the palaeobotanical evidence for exten­ sive forests and woodlands in western North America in the Early Tertiary . The first hypsodont equids are included within Merychippus (sensu lato) from the Middle Miocene, some 17- 18 Ma . Their habitat should probably be characterized as savanna woodland rather than open grassland, judging by the palaeobotanical evidence and by the fact that most contemporary ungulates (oreodonts, camels, protoceratids, dromomerycids, tapirs, rhinos, chalicotheres) had low-crowned den­ titions . By 12 Ma, however, the Merychippus stock had diversified to such an extent that fossil beds in the central Great Plains frequently contain as many as five additional genera of 'grazing' horses [Protohippus, Pliohippus, Calippus (Fig . 2), Pseud­ hipparion, Neohipparion] as well as three 'browsing' genera (Anchitherium, Hypohippus, Megahippus), which are essentially much enlarged but otherwise little modified derivatives of the Oligocene Mio­ hippus . Parahippus, morphologically intermediate between the 'browsing' and 'grazing' groups, is also found in the same death assemblages, making the Late Middle Miocene the time of greatest generic diversity within the Family Equidae . Stratigraphic­ ally higher deposits in the same area exhibit sedi­ mentological and palaeobotanical evidence for a drier climate, fewer trees and more extensive grass­ land, facts that accord well with the extinction of the last genus of browsing horse 9 Ma, when eight well demarcated hypsodont genera were still thriving . It is perhaps during this interval that the closest analogies can be drawn between North American savanna ecosystems and those of modem Africa (Webb 1983) . Later Miocene deposits (5 - 8 Ma) re­ cord increasing aridity and further restriction of woodlands in the Great Plains . Selective extinctions of browsers occurred (all North American rhinos, dromomerycids, protoceratids, and gelocids) and hypsodont taxa also declined in diversity; all but two generic lineages of horses became extinct. By the Early Pliocene, surviving equids included only Equus (which remained abundant through the Pleistocene in North America and into the Recent of the Old World as zebras, asses, and horses) and Nannippus (a diminutive, extremely hypsodont form that probably still retained lateral digits) which became extinct at the end of the Pliocene .

1 . 1 1 Grasslands and Grazers

87

2 Skull of extinct North American horse, Calippus, in palatal view showing laterally expanded muzzle and linear arrangement of incisors, presumably an adaptation for close cropping of siliceous grasses at ground level . Cheek teeth are prismatic, hypsodont, and heavily invested with cement in this genus, further indications of a grazing habit. Calippus was the first equid to evolve cheekteeth with a hypsodonty index (height/length of unworn teeth) exceeding 2.5, achieving this by the Middle Miocene, 14 Ma. It may not be coincidental that proboscideans (both mastodons and gomphotheres) reached North America at almost exactly the same time; like modern elephants, these early tuskers probably opened up areas of forest and woodland, thus encouraging the spread of grasslands and grazers . Fig.

The Late Tertiary decline of the Equidae has been much discussed. Some authors have pointed to parallel increases in diversity and abundance of contemporary ruminants (bovids, antilocaprids) and have suggested a causal relationship, attribu­ ting the differential evolutionary success of the cloven-hoofed ungulates to their remarkable ability to digest cellulose in the forestomach . Equids, in contrast, with their 'hindgut fermentation' were considered less efficient. Recent studies have com­ plicated the picture, however . It appears that in some situations - namely an overabundance of high-fibre, low quality grass - horses may be more efficient than ruminants in utilizing grasslands (Janis 1984) . Perhaps this accounts for the fact that horses, despite their decline in generic diversity, continued numerically to dominate Great Plains assemblages of large mammals from the Pliocene until well into the Late Pleistocene .

References Janis, C . M . 1984. The use of fossil ungulate communities as indicators of climate and environment. In: P. Brenchley (ed. ) Fossils and climate, pp . 85 - 1 04 . John Wiley & Sons, New York. Palmer, P . G . 1976. Grass cuticles: a new paleoecological tool for East African lake sediments . Canadian Journal of Botany 54, 1725 - 1 733. Rensberger, J . M . , Forsten, A. & Fortelius, M. 1984. Functional evolution of the cheek tooth pattern and chewing direction in Tertiary horses. Paleobiology 10, 439 -452. Thomasson, J.R. 1987. Fossil grasses : 1820- 1 986 and beyond . In: T. R. Soderstrom, K. W. Hill, C . S. Campbell, et al. (eds) Grass systematics and evolution, pp. 159- 167. Smithsonian Institute Press, Washington. Webb, S . D . 1977. A history of savanna vertebrates in the New World. Part I: North America. Annual Review of Ecology and Systematics 8, 355 - 380. Webb, S . D . 1983. The rise and fall of the late Miocene ungulate fauna in North America. In: M . H . Nitecki (ed . ) Coevo­ lution, pp. 267-306. University of Chicago Press, Chicago. Wright, V.P. (ed . ) 1986 . Paleosols, their recognition and inter­ pretation. Blackwell Scientific Publications, Oxford .

1 . 12 Hominids R. L . S U S M A N

Early hominids

been much larger than their gracile counterparts, the former may have been larger only with respect to their jaws and teeth; body weight in the two groups did not differ as much as their jaws and teeth might suggest. New palaeontological evidence uncovered at the Swartkrans, South Africa, suggests that P. robustus possessed a hand that was morpho­ logically capable of human-like precision gripping, and may have used bone and stone tools to procure plant foods (Susman 1988) . P. robustus was essen­ tially a ground-dwelling, bipedal hominid - more adapted to life on the ground than either A. afarensis or A. africanus . The latest surviving members of this robust lineage became extinct 1 .2 Ma . Contemporary with Paranthropus were the first members of the genus Homo. The earliest was Homo habilis, a species that lived mostly on the wooded savannas, in the vicinity of large lakes or along rivers . Known principally from East Africa, H. habilis had a bigger brain than either Australopithecus or Paranthropus, with an average cranial capacity of 650 - 700 cm3 . It had smaller teeth, with a premolar grinding surface of 109 mm2, and correspondingly smaller j aws and chewing muscles . Its limbs (hands, feet, and leg) and limb proportions are decidedly human-like . In many details of the foot and hand H. habilis is similar to P. robustus as well as humans. H. habilis is found with stone artifacts, and its tool tradition is known as the Oldowan (Leakey 1971 ) . The Oldowan consists primarily o f flake-tools and tools made of quartzite and chert, trimmed on only one edge for the most part . There is no evidence from marks or indications of burning of animal bones at H. habilis sites to suggest that hunting was a major subsistence activity at this stage . At the same time plant remains (including pollen) at some sites indicate that plant food gathering was still a major occupation .

Hominid evolution begins roughly 4 Ma with the first bipedal ape-men and ends with the origin of our own species (Fig. 1 ) . The first stage is character­ ized by the appearance of Australopithecus afarensis, an ape-man that lived between 4 and 3 Ma in Eastern Africa . A. afarensis was highly sexually dimorphic, with males weighing as much as 80 kg and females as little as 30 kg . These earliest hominids had small brains (350 cm3 ), long upper limbs and short lower limbs compared with later hominids; their fingers and toes were long and curved by human standards . Many anatomical features suggest that a t this stage of hominid evolution our ancestors still climbed trees while, at the same time, they were becoming bipedal (Stem & Susman 1983) . There is no archae­ ological record at this time nor is there any anatom­ ical evidence from the hand of A. afarensis that these early hominids used bone or stone tools . Between 3 and 1 . 75 Ma there is a profusion of hominid species, including Australopithecus africanus, Paranthropus robustus, P. boisei, and Homo habilis . A. africanus had a brain size of 450 - 500 cm3 (measured in six individuals) and weighed, on average, around 50 kg (females c. 30 kg and males up to 65 kg) . A. africanus was notable in having very large teeth, particularly the premolars and molars which are used to grind food; the surface area of premolars averaged 123 mm2 , compared to 107 mm2 in the premolars of A. afarensis . While some authors view A. afarensis and A. africanus as very similar (and perhaps even members of the same species), others maintain that A. africanus is the successor to A. afarensis . Morpho­ logically, there are good reasons to conclude that A. afarensis was both specifically distinct from, and ancestral to, A. africanus . These include a pro­ gression in brain size, an increase in tooth surface area, and changes in the hip which may reflect an increasing (but not yet complete) reliance on bipedalism as a means of moving on the ground . P. robustus occurs slightly later in the fossil record (> 2 - 1 . 2 Ma) than A. africanus . Paranthropus had huge teeth with premolars of 179 mm2 , and a brain averaging 500 - 550 cm3 . Although these robust aus­ tralopithecines are traditionally considered to have

Homo erectus

At roughly 1 . 5 Ma H. erectus appears in the fossil record . H. erectus, thought to be the successor to H. habilis, represents a major adaptive shift . H. erectus is found throughout the Old World, from Africa to Europe and the Far East . There is a considerable

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1 Phylogeny of Plio-Pleistocene hominids from the earliest, Australopithecus afarensis (> 3 Ma) to the most recent, modern humans (Homo sapiens sapiens) . Hominids continued to exhibit climbing adaptations until the appearance of H. erectus . Stone tools are firmly documented at c. 2 Ma (and may date back to 2.4 Ma) and were used by Paranthropus, as well as H. habilis and their descendants . The placement of A. africanus on the tree is equivocal.

Fig.

increase in body size at this stage, a reduction in sexual dimorphism and in tooth size, and a con­ siderable expansion of the brain . The skull of H. erectus is characterized by a very thick braincase with a volume of 1 100 cm3 , a long, low profile, very thick brow ridges, a well developed ridge on the occipital bone, a skull that has its widest diameter low down on the vault, and the absence of a chin . With the advent of H. erectus there was a shift in subsistence from vegetarianism (and perhaps some scavenging) to hunting. Also at this time the first clear associations of hominids and charred animal

bones occur suggesting that H. erectus used fire to prepare, and possibly cook and/or preserve game . The stone artifacts recovered with H. erectus show technical improvement over the earlier Oldowan . This stage of cultural evolution has been called the Acheulean, and is characterized by large (35 cm long) hand axes. Although in Asia and Eastern Europe a modified Oldowan (pebble-chopper) in­ dustry persists into H. erectus times, in Africa and Western Europe hand axes characterize the Acheulean industry. Hand axes were made by flaking a stone core on two sides and creating a tool

90

1 Major Events in the History of Life

that was sharp over most or all of its circumference . These tools not only indicate enhanced skills in perceiving a final form unlike the shape of the raw stone, but also greater selectivity in the choice of raw materials . As the Acheulean industry pro­ gressed, there is evidence of refined flaking tech­ niques and the use of soft hammers including wood, horn, and bone . Use of soft hammers allowed the manufacture of finer edges on cutting and chopping tools . The remains of selected large mammals with cut marks, and indications of burning at H. erectus sites, suggest that hunting was a major subsistence activity at this stage . At the same time plant remains (including pollen) at Acheulean sites indicate that plant food gathering was still a major part of the subsistence activity of H. erectus.

Archaic Homo sapiens The H. erectus grade existed for more than one million years . Their successors have been called archaic H. sapiens, and early representatives have been unearthed principally in Africa and Europe . Fossils indicate that b y 300 000 years ago the earliest H. sapiens had spread throughout the Old World . There are conflicting views as to where H. sapiens originated from its geographically dispersed prede­ cessor, H. erectus. Some suggest that local popu­ lations of H. erectus in different parts of the world evolved separately into the different races of H. sapiens. Another theory is that only a single popu­ lation gave rise to H. sapiens and that this population eventually replaced the others . Confounding a better understanding of this phase in hominid evolution is a dearth of both firm radio-metric dates and good archaeological sites, and the fragmentary condition of hominid fossils. Fossils from this time period include a distorted skull from Steinheim, West Germany, a partial braincase from Swanscombe, England, a skull from Kabwe, Zambia, and a partial skull from Bodo, Ethiopia . The cranial volume of archaic H. sapiens reached 1200 - 1300 cm3 (within the range of modern humans) . The braincase is also thinner than that of H. erectus, with a somewhat higher forehead and a shorter face . The stone tool industry associated with archaic H. sapiens indicates that as early as 500 000 years ago Acheulean tools became smaller and at 220 000 years ago a new technological innovation was introduced . The new method o f tool making consisted o f first preparing a cylindrical core, then striking long blades from it. This is known as the Levallois tech-

nique, and the new culture, called the Mousterian, first appears in Europe. The Mousterian is thought to have evolved from the advanced Acheulean. The transition from Acheulean to Mousterian was a gradual one, with considerable overlap between them.

The Neanderthals Following the archaic H. sapiens of the Middle Pleistocene came the Neanderthals . One popular definition of Neanderthal is that group of hominids that occupied Europe and the Near East from 100 000 to 40 000 years ago . This stage is known from frag­ mentary skeletal remains of only 100 or so indivi­ duals . Neanderthals are distinguished from earlier archaic H. sapiens by their thin skull, rounded fore­ head, reduced brow ridges, prominent, broad nose, rounded orbits, flattened cheek bones, enlarged cranial volume (1500 cm3 and more), large pulp cavi­ ties in their small molar teeth, and a space between their last molar tooth and the vertical part of the jaw bone . Some Neanderthal skulls had a bun on the back where neck muscles attached, but others lacked this feature . Some Neanderthal jaws had a very weak chin, while others had a prominent mental eminence . Neanderthals were stockily built, with very thick-walled long bones even in the very young. The Mousterian culture is closely associated with Neanderthals of the later Pleistocene, a period marked by increased cultural diversity. There were dozens of different types of stone implements in the Mousterian tool kit . Very specialized blade-tools were fashioned from pre-flaked cores, and pressure flaking was used to sharpen their edges. The Mousterians hunted large mammals and gathered plant foods . Our knowledge of their subsistence is aided by the fact that Mousterian artifacts and Neanderthal remains are found in cave sites (unlike earlier excavations of archaic H. sapiens that are found in fluvial deposits and in open-air sites) . Archaeological evidence reveals that Nean­ derthals buried their dead . Evidence of magico­ religious beliefs comes from excavated grave goods. Hunting practices involved the exploitation of re­ latively few large species and the year round oc­ cupation of sites (rather than seasonal migration) . Other cultural practices included the construction of shelters, the application of surgical procedures to the sick and injured, and the widespread, use of fire . Around 40 000 years ago Neanderthals disappeared from the fossil record .

1 . 12 Hominids Modem humans The remains of modem humans in the Upper Palaeolithic are far more common than those of Neanderthals, because of the increased practice of burying the dead . Hominid fossils in the 40 000 year time range are virtually indistinguishable from modem humans (some earlier remains dated c. 90 000 are also very modem looking) . They had small, broad, non-projecting faces, high foreheads, protruding chins, and large (1500 cm3) cranial ca­ pacities . Their stature was similar to that of modem humans, in the 1 68 - 182 cm range . Jaws and teeth recovered from Europe suggest that they had widely varying diets . There are also Upper Palaeolithic fossil remains from Asia, Africa, and the Pacific . Modem humans of the Upper Palaeolithic pos­ sessed a range of stone tool industries . The refined Upper Palaeolithic industries produced blade tools that were finished by soft hammers and pressure, rather than percussion flaking. Many of the stone tools were hafted onto arrow or spear shafts; other projectile points were made from bone and tusk. Scrapers, borers, and small cutting tools were fashioned for the preparation of shafts, skins, as well as food-stuffs . Humans of the Upper Palaeolithic hunted, fished, and gathered plant foods in a wide range of environ­ ments from warm and humid to cold climates . In some areas, such as Northern Europe, there is evi­ dence of seasonal exploitation of migrating game . Fossil evidence also reveals that rhinoceros, mam-

91

moth, and bear were hunted . In coastal areas there was heavy exploitation of marine resources . At two sites in Germany over 99% of the mammalian faunal remains consist of reindeer. There is a considerable amount of cave art and plastic art beginning about 30 000 years ago in Europe . The functional significance of cave and chattel art has been debated but most subscribe either to the theory that art is related to hunting rituals occasioned by periodic (seasonal) short­ ages of food, or that the symbolism had sexual­ reproductive connotations . Humans in the Upper Palaeolithic survived injur­ ies and disease to a greater extent than earlier homi­ nids. The life expectancy of humans in the Upper Palaeolithic had improved over that of the earlier Neanderthals, although it was still low by modem day standards . Roughly half of European and Asian individuals reached the age of 21 years, and only 12% reached 40 years old .

References

Leakey, M . D . 1971 . Olduvai Gorge. Volume 3: Excavations in beds I and Il, 1 960 - 1 963 . Cambridge University Press, Cambridge . Stern, J.T. & Susman, R.L. 1983. Locomotor anatomy of

Australopithecus afarensis . American Journal of Physical Anthropology 60, 279 - 317. Susman, R L . 1988 . The hand of Paranthropus robustus from Member 1, Swartkrans : fossil evidence for tool behavior. Science 240, 781 - 784.

2

T H E E V O L UT I O N A RY PRO CESS AND THE F O S S I L RE C O RD

The Ordovician trilobite Ogygiocarella, x 1 . 35 . (Photograph courtesy of P.R. Sheldon.)

2.1 Molecular Palaeontology G . B . C URRY

Introduction

ganic molecules can survive for many millions of years has been one of the most remarkable geologi­ cal discoveries of recent years (see also Section 3 . 2) . The presence o f large quantities of organic debris in rocks has long been recognized, but previously it had been widely assumed that these compounds contained no palaeontological or biological infor­ mation because of the extensive degradation they had experienced . It is now clear that such an assumption is wrong, and that certain robust mol­ ecules can survive virtually intact, or at least in recognizable form, for many millions of years . The key to such discoveries lies in the application of technological advances in subjects such as organic geochemistry and molecular biology which allow the recovery, purification, and characterization of organic materials with a precision never before attainable (Curry 1987) . The raw material for molecular palaeontology is the accumulation of the variably decayed remains of ancient animals, plants, and micro-organisms which has built up in rocks over many millions of years (Section 3 . 2) . This organic debris occurs both interstitially in sedimentary rocks and as inclusions within fossil shells and skeletons . The vast scale of such accumulations is perhaps not generally appreciated - enormous as they are, the reservoirs of fossil fuels such as oil, gas, and coal represent only the tip of the iceberg. To a greater or lesser extent all sedimentary rocks contain less apparent, highly dispersed, and generally less degrad ed, or­ ganic debris . On average about 2% of the volume of sedimentary rocks is composed of organic com­ pounds, and conservative estimates suggest that there is about 10 000 times more organic material in rocks than in the present-day global biomass . One group of ubiquitous molecular fossils, the bio­ hopanoids, is present in quantities which equal or exceed the total mass of organic carbon in all living organisms . Most of this reservoir is thought to be useless for molecular palaeontology, because it has been so intensely altered as to be totally unrecognizable . In addition to the complications imposed by hydro­ lyzation and other physical, chemical, and biological

In its widest sense, molecular palaeontology em­ braces the study of intact molecules in living organ­ isms, as well as the investigation of the variably decayed remnants of ancient molecules which occur in great abundance in rocks and fossils (Runnegar 1986) . In extant molecules such as DNA or proteins, the nucleotide or amino acid sequences are repro­ duced accurately from generation to generation with only minor changes caused by genetic drift or natural selection . Because such molecules are ubiquitous in all life forms, homologous molecules can be extracted from a wide taxonomic range of living organisms and their sequences compared, either directly or indirectly, to provide information on the systematic interrelationships of their host organisms . Using such techniques, phylogenetic history can be investigated on a scale ranging from phyla to subspecies . The molecular clock hypothesis further extends this approach by attempting to use molecu­ lar 'distances' to date divergent events between taxa (Thorpe 1982) . To do this the molecular clock must first be calibrated using sequences from organisms which have well dated divergence events - in effect organisms which have a good fossil record . The molecular clock hypothesis is hotly debated even by molecular biologists, and it is clear that the rates of sequence change are highly variable both in different molecules and in identical molecules within different species . Nevertheless, the interest in the molecular clock does mean that molecular biologists will increasingly be drawing conclusions and making predictions about topics which previously have been the exclusive preserve of palaeontologists .

Fossilization of organic molecules Despite the palaeontological importance of recov­ ering the prodigious 'historical' information stored in extant molecules, it is undoubtedly the investi­ gation of molecular fossils which has the greatest potential for the development of molecular tech­ nology in palaeontology . The fact that resistant or-

95

96

2 The Evolutionary Process and the Fossil Record

processes of decay, investigations of molecular fos­ sils have also to contend with the effects of a host of other geological phenomena such as diagenesis, vulcanism, and tectonism . As a result, fossil mol­ ecules can be exposed to an infinitely variable com­ bination of heat, pressure, and percolating fluids, and can with time recombine into complex and intractable new structures by reacting with each other and with mobile components migrating from external sources . The possibility of contamination by molecules derived from extant organisms is an additional, and ever-present, complication . In the face of all these problems, the extent to which molecules can survive fossilization is strik­ ing, most particularly in the well documented cases of molecules which are fully exposed to the ravages of geological processes . The commercial impli­ cations of accumulations of fossil molecules has provided a major stimulus for their study, and a wide range of molecular fossils have now been discovered in crude oils which have been intensely degraded . The great majority of fossil organic ma­ terial has not been so intensely degraded, and hence should be particularly informative, although as yet such material has not been thoroughly investigated .

Analytical techniques The major complications in investigating molecular palaeontology stem from the fact that raw samples contain extremely complex assemblages of molecu­ lar fossils, which occur in all stages of decay, from virtually unaltered to strongly degraded . Further­ more, most liberated fossil compounds readily com­ bine into complex, heterogeneous agglutinations, which are often insoluble and hydrophobic and hence difficult to analyse . The first hurdle, therefore, is to separate the different constituents, and to recognize the various stages in the decay of a par­ ticular molecule, each of which will generally produce slightly different daughter products de­ pending on its decay history. The development of chromatographic and electrophoretic techniques which can reliably separate and analyse samples of 1 flg or less provided a major stimulus to the study of organic debris within fossils, although the long-term survival of molecular fossils was first demonstrated using techniques from organic geochemistry . Organic chemists now derive most of their infor­ mation from computer-controlled combined gas chromatograph mass spectrometers (C-GC-MS) which first separate, and then analyse, the structure

of fossil molecules at a resolution measured in nano­ grams (10- 9 gm) . These procedures can identify geochemical fossils because the carbon skeleton of the original biological molecule is characteristically preserved either unaltered or with minor rearrange­ ments, substitutions, or the removal of side chains (Fig. 1 ) . A significant recent technological advance is the recognition that large, highly reactive mol­ ecules, which are usually particularly susceptible to degradation, can be stabilized over geological time when incorporated into inert polymeric aggluti­ nations . These relatively intact and extremely informative fossil molecules can be released by the partial chemical dissolution of fossil polymers prior to C-GC-MS analysis, and have now been isolated from well preserved 50 Ma compounds . The main drawback to the organic geochemical approach is that the analytical techniques are complex and re­ quire specialist skills and expensive equipment. The major preoccupation of molecular palaeon­ tology has been to demonstrate unambiguous links between intact living molecules and their resistant fossil remains . A classic example is the petropor­ phyrins, which are common constituents of crude oils. As early as 1934 it was proposed that vanadyl petroporphyrin represented degraded chlorophyll A from plants; the fossil molecule has essentially the same structure, but has lost its side chain and the central magnesium ion has been substituted by a vanadyl ion (Fig. 1 ) . Subsequently the decay pathways of a wide range of compounds have been traced from living organ­ isms through to sediments and rocks, providing information both on the origins of fossil fuels and on the conditions which prevailed during their alteration (because the state of decay is closely re­ lated to temperature, pressure, etc . ) . Molecular fos­ sils can also provide information about ancient environmental conditions, e . g . when the chemical composition of a group of marine phytoplankton is known to vary directly with ocean temperature, and such variations can be detected in their fossil re­ mains . Mapping out the distribution of such com­ pounds in rocks therefore provides some indication of oceanic temperature variations in the past . Investigations of fossil molecules have also led to the discovery of previously unrecognized living molecules; biohopanoids, an important group of membrane-forming lipids in extant bacteria, were first recognized by their ubiquitous fossil derivatives .

2 . 1 Molecular Palaeontology

C h lorophyl l A

Vanadyl porphyrin

1 A classic example of a geochemical fossil - vanadyl porphyrin, one of a suite of petroporphyrins (common constituents of crude oils), which is thought to be the breakdown product of the photosynthetic pigment chlorophyll A from plants . Over geological time the central magnesium ion has been replaced by a vanadyl ion, and the side chain has been stripped away. The side chains of chlorophyll are thought to give rise to other common geochemical fossils (phytanes and pristanes) . Fig.

Organic compounds from biominerals There is now considerable interest in the preser­ vation of molecular fossils within the shells and skeletons of fossils (Wyckoff 1972; De Jong et al. 1974; Westbroek et al . 1979; Hare et al. 1980) . Compared with free compounds in sediments and rocks, organic compounds from biominerals are relatively protected from decay and con­ tamination - a kind of biological 'fluid-inclusion' . It is widely believed that this important group of

97

molecular fossils represents the remains of original organic compounds which were incorporated into the skeletal fabric during shell growth as essential extra- or intracrystalline elements of 'organic­ matrix-mediated' biomineralization . Although these entombed molecules do fragment over geo­ logical time, it is now clear that some of their breakdown products are often retained within skeletal fabrics (Figs 2, 3) . The more porous mineral­ ized matrices are obviously much more prone to contamination from percolating fluids, but the possibility of spurious results can be reduced by investigating the organic content of surrounding sediment, and by determining stable carbon isotope ratios which reveal the contamination of marine fossils by predominantly terrestrially-derived groundwater. Palaeontologists have long been interested in biomineralization processes, and an understanding of the intimate association between the organic matrix and the inorganic mineralized phase, which appears to be a major factor in the long­ term stability of molecular fossils, is clearly crucial for the full exploitation of molecular palaeontology . Organic compounds have now been isolated and characterized from a diverse taxonomic range of invertebrate and vertebrate fossils spanning the en­ tire history of shelly faunas (i . e . 600 million years) . The best results have been obtained with well pre­ served Mesozoic, Cenozoic, and Quaternary speci­ mens (i . e . the past 250 million years) . These data have mostly been presented in the form of amino acid mole percentages . Detailed analyses o f molecular remnants from living and fossil scallops spanning about 200 million years demonstrate the expected progressive decay in the total quantity, and percentage survival, of amino acids (Fig . 2) . The rate of decay reaches a plateau at about the 1 % - 2% survival level during the Cretaceous (c. 100 million years), and thereafter the total quantities of molecular fossils remain rela­ tively constant . Free amino acids represent only one of three broad categories of molecular fossils recognized; insoluble organic residues and soluble peptides also display a similar decay profile (Fig . 3). Changes in the respective proportions of these components with time probably indicate some movement between categories . The consistency of amino acid profiles over geological time is remarkable, for example in nautiloids spanning almost 400 million years . Changes in relative abundance with time are gener­ ally thought to be a diagenetic effect, and such alteration phenomena are useful indicators of the

2 The Evolutionary Process and the Fossil Record

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state of fossil preservation when coupled with iso­ topic data and laboratory experimentation on Recent shells.

Molecular fossils and systematics Because of the ubiquitous distribution of amino acids in living tissues, the amino acid compositions

of fossils have as yet had only limited use as taxo­ nomic indicators . However, consistent differences between the amino acid compositions of living and fossil brachiopods appear to distinguish between brachiopod orders, with the chitinophosphatic­ shelled inarticulate Lingula being characterized by higher concentrations of alanine and lower glycine . While such variations are probably related to differ­ ent shell mineralogy, amino acid profiles also distinguish between different orders of calcareous­ shelled articulate brachiopods . It seems highly prob­ able that the crude systematic application of such data will be restricted to the higher levels of taxonomic classification (i. e . superfamily, order) . A more recent innovation has been the use of immunological techniques to investigate molecular fossils (De Jong et al. 1974; Westbroek et al. 1979; Muyzer et al. 1984; Lowenstein 1986) . Such an appli­ cation makes use of the major attribute of the im­ mune system, namely that antibodies recognize their target molecule by detecting a small diagnostic region or regions known as determinants . Anti­ bodies prepared against living tissues or a particular fundamental molecule such as collagen, can there­ fore detect the presence of that molecule in fossils, provided that fragments containing the determi­ nants have survived . As determinants are much smaller than intact molecules, their survival poten­ tial is much greater. Antigenic determinants are known to survive for at least 70 million years (De Jong et al. 1974; Lowenstein 1986) . The advantages of immunology are the high specificity of antibodies

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2 . 1 Molecular Palaeontology (in particular monoclonal antibodies directed against a single molecule), and the ability to carry out large numbers of determinations once the antibody has been prepared, which allows rapid assessments of the extent of fossil organic preservation . The pro­ duction of antibodies is, however, a complex and specialized field . Immunological techniques potentially provide greater systematic resolution, at least to the generic and familial level, although species-specific reac­ tions have been detected in relatively recent fossils (Lowenstein 1986) . Such an application is in effect a variation of the widely used technique of recon­ structing phylogeny from immunological distances, a procedure which can be justified on the grounds of the direct linear relationship between antigenicity and amino acid substitution rate . Experiments with living taxa have demonstrated the potential of im­ munology in this field, with antibodies against one bivalve species reacting with all but one of the other taxa in its family; the implication that the excep­ tional genus may be incorrectly assigned is appar­ ently supported by other lines of evidence (Muyzer et al. 1984) . Full exploitation of the evolutionary and taxo­ nomic applications of molecular palaeontology will require much more detailed information about the structure, composition, survival potential, and dis­ tribution of fossil molecules . Although there have been reports of the preservation of fragments of DNA in 2000 year old mummies and other relatively recent fossils, DNA molecules are relatively un­ stable, particularly susceptible to hydrolysation, and concentrated in vulnerable soft tissues rather than protective mineralized skeletons (Runnegar 1986) . On present information, DNA is therefore likely to be very short-lived on a geological time-scale, although extant DNA is a potent source of infor­ mation for palaeontologists . The search for molecu­ lar fossils must, at least for the present, concentrate on the more or less informative building blocks of organic molecules produced by DNA (e . g . protein residues) as a pathway to the partial understanding of the composition of ancient biochemical systems . Certainly the widespread preservation of amino acids, and the more restricted survival of appreciable portions of original molecular structure for at least 70 million years, has been demonstrated by immu­ nology and organic geochemistry . The extent of such excellent preservation is unknown, however, and at the present time the field is one of consider­ able potential, tantalizingly glimpsed but with little hard data .

99

Reports of the preservation of characteristic ori­ ginal amino acid sequences of 80 Ma fossil shell proteins are particularly encouraging, as is the re­ ported (but not published) sequencing of 15 amino 2 acids at the N terminal end of a small Ca + binding protein from oyster shells of Recent, Middle Miocene (15 Ma), Middle Cretaceous (100 Ma), and Middle Jurassic (175 Ma) ages . However, it has so far proved extremely difficult to sequence segments of fossil molecules routinely, perhaps because of inter­ ference from co-existing dark polymeric com­ pounds . Technological developments which are much more precisely tailored for the special con­ ditions of the fossil record are clearly crucial, and palaeontologists may well have to become more familiar with the capabilities of existing equipment and possibly even involved in the design of new equipment . Whatever the technique, it is clear that an inte­ grated approach is necessary to avoid the many potential pitfalls in working with molecular fossils . Taxonomic studies should, in the first instance, concentrate on organisms which have a long and abundant fossil record and are still living today . This allows cross-checking of phylogenetic infer­ ences against morphology, extant biochemical sys­ tematics, and geological history, and the tracing of organic preservation from living to fossil within single lineages . Large numbers of well preserved specimens of different ages are required, since the yield of organics per gram of fossil is low . A robust, non-porous, coarsely-crystalline, skeletal ultrastruc­ ture is also an obvious advantage because of the protection it provides for enclosed molecular fossils . At the present state of knowledge only high level taxonomic indicators can realistically be anticipated from molecular fossils, and the most obvious and dramatic demonstration of such an application may well come from problematic groups whose mor­ phology provides ambiguous clues as to their taxo­ nomic affinities . In any event it is certainly now possible to begin utilizing fossil molecular data to augment or complement existing taxonomic meth­ odology . All of the taxonomic tools available to the palaeontologist, including the study of morphology alone, have particular strengths and weaknesses; taken in combination, molecular and morphological, living and fossil, they will be a potent measure of taxonomic relationships .

Future developments The assimilation of such complex and unfamiliar

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2 The Evolu tionary Process and the Fossil Record

technology into geological investigations is neces­ sarily a slow procedure, but the investigation of molecular palaeontology is now a blossoming field . Although molecular data from the fossil record is still beyond the grasp of most scientists, the speed of development, and of automation, is such that analyses of this kind may soon be routine . Current studies have clearly demonstrated that such work can significantly augment or complement a wide diversity of geological and biological research . In addition to taxonomy, there are, for example, indi­ cations that the remains of ancient molecules also contain important information on geochronology (i . e . amino acid dating), the origins of fossil fuels, palaeoenvironment reconstructions, and the pro­ cesses which operate during diagenesis . For the biologists such organic remnants could well provide valuable in sights into evolutionary processes at the molecular level .

De Jong, E . W . , Westbroek, P., Westbroek, J . F . & Bruning, J.W. 1974. Preservation of antigenetic properties in macro­ molecules over 70 myr old. Nature 252, 63 - 64. Hare, P . E . , Hoering, T . e . & King, K. (eds) 1980 . Biogeo­ chemistry of amino acids . John Wiley & Sons, New York. Lowenstein, J.M. 1986. Molecular phylogenetics. Annual Review of Earth and Planetary Sciences 14, 71 - 83 . Muyzer, G . , Westbroek, P . , d e Vrind, J . P . M . , Tanke, L Vrijheid, T . , De Jong, E . W . , Bruning, J.W. & Wehmiller, J . F . 1984. Immunology and organic geochemistry. Organic Geochemistry 6, 847-855. Runnegar, B . 1986 . Molecular palaeontology. Palaeontology 29, 1 - 24. Thorpe, J . 1982 . The molecular clock hypothesis : biochemi­ cal evolution, genetic differentiation and systematics. Annual Review of Ecology and Syetematics 13, 139 - 168. Westbroek, P., van der Meide, P . H . , van der Wey-Kloppers, J . 5 . , van der Sluis, R.J . , de Leeuw, J.W. & De Jong, E.W. 1979 . Fossil macromolecules from cephalopod shells: characterization, immunological response and diagenesis . Paleobiology 5, 151 - 160. Wyckoff, R.W.G. 1972 . The biochemistry of animal fossils . Scientechnica, Bristol.

References Curry, G . B . 1987. Molecular palaeontology: new life for old molecules. Trends in Ecology and Evolution 2, 161 - 165.

2.2 Speciation B . C H A RL E S W O RTH

Species concepts Modern evolutionary biologists are generally agreed that the biological species concept provides the most satisfactory basis for discussing the problem of the origin of new species (speciation). According to the biological species concept, species are 'groups of actually or potentially interbreeding natural popu­ lations which are reproductively isolated from other such groups' (Mayr 1942) . This concept was arrived at during the nineteen-thirties, as a result of the recognition by systematists and geneticists that purely morphological definitions of species are unworkable, in view of phenomena such as the occurrence of intergrading sets of morphologically distinct populations over a geographical range, and of morphologically nearly indistinguishable but re­ productively isolated populations coexisting in the

same place . Under the biological species concept, the former situation is now treated as a case of a single polytypic species or Rassenkreis, and the latter as the existence of a number of sibling species. Examples of polytypic species and sibling species abound (Mayr 1963), and demonstrate that there is no tight causal relation between the evolution of morphological differences of the kind that are de­ tectable in the fossil record, and the evolution of reproductive isolation . A polytypic species is at least potentially capable of evolving as a unit, e . g . a selec­ tively favourable mutation that arises at one end of its range is capable of diffusing throughout the whole species, as a result of migration, and replacing its alternative allele . Conversely, such a mutation has no prospect of spreading from one biologi­ cal species to another under natural conditions .

2 . 2 Speciation In this sense, the biological species represents a natural unit of evolutionary change . Clearly, the concept applies only to sexually reproducing or­ ganisms . Furthermore, cases where it is difficult to apply are observed, and are indeed to be ex­ pected, since intermediate stages in the degree of reproductive isolation between geographically or ecologically separated populations must occur under almost any evolutionary hypothesis other than that of strictly saltatory evolution (Mayr 1963) .

Modes of reproductive isolation According to this view of the nature of biological species, the process of speciation is to be equated with the development of reproductive isolation be­ tween two populations that were formerly fully capable of interbreeding. This process is the ulti­ mate source of the diversity of life on Earth, since sympatric populations that are not reproductively isolated will eventually lose their distinctness. Modes of reproductive isolation may be divided into the two broad categories of prezygotic and postzygotic barriers, referring to whether or not F1 hybrid individuals are produced by matings be­ tween members of the two species (Dobzhansky 1937; Mayr 1963) . Prezygotic modes of isolation include differences in ecology, timing of breeding or flowering, and differences in mating behaviour or reproductive physiology, that prevent success­ ful fertilization in interspecific matings . In many groups, such as Drosophila, behavioural prezygotic isolating barriers are the primary agents that pre­ vent gene flow between sympatric species, which are often completely isolated genetically in spite of the absence of strong postzygotic barriers (Coyne & Orr 1989) . Postzygotic isolating barriers include inviability or sterility of F1 individuals, or of sub­ sequent hybrid generations . Theoretical studies have shown that isolating bar­ riers have to be extremely strong in order to prevent gene flow between two populations that are in contact . Neutral alleles will face no significant obstacles to diffusion from one population to the other unless there is nearly a 100% loss in fitness to F1 hybrids, or their probability of formation is near zero, except for loci which are very closely linked to genes involved in controlling the isolating mechan­ isms (Barton & Charlesworth 1984) . The same ap­ plies to alleles that are selectively advantageous in both populations, but originally arise by mutation in only one of them . Studies of hybrid zones, where two genetically distinct geographical races come

101

into contact along a linear transect, resulting in a relatively narrow region where hybrids are formed, have demonstrated empirically that such gene flow occurs at enzyme and protein loci detected by elec­ trophoresis (Barton & Charlesworth 1984) . These are probably close to being selectively neutral . Loci that are under natural selection that favours differ­ ent alleles in the two populations (because of differ­ ences in environment or genetic background) may remain differentiated between populations in con­ tact; the extent of such divergence depends on the balance between the strength of the selection pressure concerned and the amount of gene flow . Clines, where populations vary along a linear tran­ sect in response to an environmental gradient in selection pressure, are the product of such a bal­ ance (Endler 1977) . There are numerous examples of clines maintained over very short geographical gradients by intense selection pressures, the classic example being the evolution of metal tolerance by plants living on polluted sites such as old mine spoils (Endler 1977) . There is thus no difficulty in understanding how morphological and physiologi­ cal differences can be maintained between popu­ lations that are more or less freely exchanging genes, and which show little differentiation with respect to protein loci . These populations do not constitute separate species . Knowledge o f the genetic basis o f isolating bar­ riers between species is clearly of crucial import­ ance in understanding the ways in which they may evolve . In flowering plants, it seems that ecological differences between related species often prevent interbreeding between them, even if they inhabit the same general area; habitat disturbances may result in the mingling of populations isolated in this way . There is clearly no direct genetic control of reproductive isolation in these cases, other than via the characters that lead to the ecological differ­ ences between the species . Such differences seem to be under the same type of genetic control as similar within-species differences (Stebbins 1950) . This is generally true of morphological and physio­ logical differences between related species (Mayr 1963; Barton & Charlesworth 1984) . Genetic analysis of behavioural isolating barriers has largely been confined to Drosophila. What little information is available indicates that these are usually polygenic in nature, with different loci controlling male and female courtship behaviour (Barton & Charlesworth 1984) . The genetic basis of sterility or inviability of inter­ species hybrids has been much more thoroughly

2 The Evolutionary Process and the Fossil Record

102

studied . Especially in plants, differences in chromo­ somal arrangements between related species often result in reduced pairing between chromosomes at meiosis in Fl hybrids, leading to the production of gametes containing abnormal numbers of chromo­ somes (Stebbins 1950) . Zygotes resulting from these gametes suffer reduced viability, so that the effective fertility of the hybrid is low . Accidental doubling of the chromosome number in an interspecies hybrid can lead to restoration of fertility, in cases where failure of pairing of chromosomes in meiosis causes hybrid sterility in diploids, since tetraploidy allows pairing between homologous chromosomes derived from the same species (Fig. 1 ) . Crosses between such tetraploid hybrids and the parental species result in the production of sterile triploid individ­ uals, so that the former are effectively a new species. Polyploidy of this kind is an important mode of speciation in flowering plants (Stebbins 1950), and is the only known method of saltatory speciation other than by the spread of a parthenogenetic vari­ ant within an originally sexual population . Fl sterility due to failure of proper development of the gonads or germ cells, rather than failure of chromosome pairing, is a common phenomenon in animals and plants . In animals with separate sexes and chromosomal sex determination, it has long been known that it is often the heterogametic sex (i . e . the sex that is heterozygous for the chromosome pair involved in sex determination) that is most severely affected (Haldane's rule) . The same rule Pa rent 1 AA BB CC

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also applies to hybrid inviability . This provides an opportunity to study the genetic basis of the ster­ ility by means of crosses involving the fertile sex . This has been extensively exploited in Drosophila (Dobzhansky 1937; Muller 1940; Coyne & Orr 1989) . The results of these studies show that sterility (or inviability) is caused by interactions between sev­ eral genes, such that combinations of alleles derived from the two different species result in sterility. The simplest situation of this kind is when one species has a genetic constitution AIBI/AIBI and the other A2 B 2/A2 B 2 , where A and B represent two different loci . Each species is, of course, perfectly fertile and viable; infertility or inviability results from adverse effects of interactions between the alleles A2 and BI or Al and B 2 • It is frequently observed that loci on the sex chromosomes themselves often contribute disproportionately to the fitness breakdown of hy­ brids . This is probably the causal basis of Haldane's rule; X-linked or Y-linked alleles from one of the two parental species are fully expressed in Fl hy­ brids of the heterogametic sex, and have the poten­ tial to interact adversely with alleles from the other species at loci on non-homologous chromosomes (Muller 1940; Coyne & Orr 1989) .

The origin of reproductive isolation These data indicate that changes at several gene loci are usually required for the achievement of reproductive isolation, other than by polyploidy or parthenogenesis . This is virtually a logical necessity, since it is most unlikely that a mutant allele at a single locus could both confer a high degree of infertility with individuals carrying the original allele, and become fixed in the population in oppo­ sition to this intense pressure of selection . The only faintly plausible mode of speciation by a single genetic change is through the chance fixation in a small population of a chromosomal rearrangement that causes drastic fertility loss to its heterozygous carriers . However, the chance of such a fixation event is very small in a random-mating population when the fertility loss to heterozygotes is high . Furthermore, even the most infertile rearrangement heterozygotes rarely suffer a fitness loss of more than 50% or so, and it has been shown that this reduction in fertility does not create much of an isolating barrier . Thus, even chromosomal specia­ tion is most likely to occur as a result of a number of steps, each of which has a small impact on fertility (Barton & Charlesworth 1984) . The empirical evidence from the genetic analysis

2 . 2 Speciation of species crosses is in good general agreement with these population genetic considerations . It should be stressed, however, that we have little idea in any individual case as to what has caused the genetic divergence between two populations that results in pre- or postzygotic isolation . A variety of theoretical models that can generate the evolution of such isolation have been proposed . As first pointed out by Darwin (1859), when criticizing the idea that hybrid sterility has evolved in order to prevent the fusion of species, post-zygotic isolation cannot be selected for directly, since natural selection can never favour lowered fitness. Dobzhansky (1937) and Muller (1940) proposed that the accumulation of independent evolutionary changes in two totally geographically isolated populations will very prob­ ably eventually result in the evolution of reproduc­ tive isolation . This can occur even if the populations are subject to identical environments, since different mutant alleles at different loci will arise by chance in the two populations, and become fixed by gen­ etic drift or natural selection. The process is facili­ tated by the existence of environmental differences between the populations, to which they become adapted . Alleles that get fixed in one population are not selected to interact well with the alleles from the other population, but have to perform well on the background of their own population. Thus, a suf­ ficiently long process of divergence will result in the establishment of gene combinations that function perfectly well within the population in which they occur, but produce a breakdown in fitness when alleles from one species are combined with those from the other . The loss in fitness to species hybrids is no more surprising than the fact that a carburettor from a car manufactured in the U . S . A . does not function in an engine made in Japan . This model is entirely consistent with the genetic evidence de­ scribed above . Furthermore, the predominant role of the sex chromosomes in contributing to the lack of fitness of Fl hybrids between closely related species is predicted by this model, if the genetic changes concerned are due to the fixation by natural selection of alleles that are favourable on the back­ ground of their own species (Coyne & Orr 1989) . Similarly, prezygotic isolating barriers can be understood as a product of the gradual diver­ gence in male and female courtship behaviour (in animals), or in the biochemistry of fertilization, between two geographically isolated populations . The male and female functions within any single population are, of course, always selected to en-

103

sure efficient mating and fertilization, but there is no such selection to preserve the ability to mate with individuals from a geographically separate population . Sexual selection, acting on mutations affecting male characteristics of relevance to suc­ cess in competition for females, may promote the divergence of isolated populations with respect to mating behaviour. An alternative possibility, first suggested by Dobzhansky (1937), is that prezygotic isolating barriers are the product of selection for behaviour patterns that prevent the gamete wastage which occurs because of matings between members of two populations that are in contact, and kept separate by postzygotic barriers (the process of re­ inforcement) . While reinforcement is a theoretical possibility, it seems unlikely to be the only cause of the evolution of prezygotic isolation, since many cases are known where this occurs between popu­ lations that have never been in contact . Further­ more, unless postzygotic barriers are very strong, it is probable that two populations in contact will merge before they evolve behavioural differences, except in systems where narrow hybrid zones are maintained or where sharp ecological gradients maintain differentiation (Fisher 1 930) . None the less, there is some evidence that reinforcement plays a role in the evolution of behavioural isolation in the genus Drosophila, since pairs of closely related Drosophila species that are sympatric tend to have stronger degrees of behavioural isolation than pairs of allopatric relatives (Coyne & Orr 1989) . The possibility that speciation may be triggered by random drift during periods of restricted popu­ lation size associated with the foundation of new, geographically isolated populations (founder effect speciation) has been the subject of considerable de­ bate (Mayr 1963; Barton & Charlesworth 1984; Carson & Templeton 1984) . The basic idea is that two alter­ native stable equilibria may occur under natural selection . The ancestral population is located at one of these equilibria, and passage through a small founding population causes random sampling of genotype frequencies that can sometimes result in a chance transition from one equilibrium to the other . Under appropriate circumstances, a hybrid popu­ lation formed from crossing populations located at the two alternative equilibria will suffer a substan­ tial fitness loss, and so the two populations will be at least partially isolated reproductively . The original motivation for this theory was the observation that populations of a species are often relatively uniform over a wide geographical range, but peripheral isolates may deviate sharply in their

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2 The Evolutionary Process and the Fossil Record

characteristics from these . This led Mayr (1963) to propose that the potential for evolutionary change is restricted in large populations, because of the existence of genetic and developmental devices that prevent the manifestation of new variation on which selection could act . He claimed that these devices can be overcome by the random genetic changes that accompany the foundation of a new, isolated population . Later, Carson was stimulated to pro­ pose a related idea by the observation that inter­ island migration of Hawaiian Drosophila is almost invariably accompanied by speciation (Carson & Templeton 1984) . While theoretical models have shown that partial reproductive isolation can indeed evolve by this mechanism, the probability of pro­ ducing anything approaching complete isolation by a single founder event is low . In addition, empirical and theoretical results of population genetics do not support the notion that evolutionary change is in­ hibited in large populations (Barton & Charlesworth 1984) . Finally, alternative interpretations of the bio­ geographical data advanced in support of founder effect speciation have been proposed . For example, complete isolation permits two populations to dif­ ferentiate with respect to favourable alleles, which would diffuse through both populations if they were connected by a chain of intermediate popu­ lations . This will produce an association between the foundation of new isolates and divergence or speciation. The role of founder events as causal agents of speciation thus remains controversial .

Sympatric and parapatric speciation So far, the discussion of mechanisms of specia­ tion has proceeded as though reproductive isolation takes place as a result of the genetic divergence of wholly isolated, geographically separate popu­ lations . This is the process of allopatric speciation, which can proceed by the mechanisms described above . There is little question that this is an impor­ tant mode of speciation, perhaps the predominant one . This view has been vigorously championed by Mayr (1942), and there is indeed a wealth of distributional evidence which suggests that geo­ graphical isolation promotes genetic divergence and speciation . The most extreme alternative is sympatric speciation, the evolution of reproductive isolation between genotypes within a population that was originally mating randomly . Theoretical models of this process are reviewed by Seger (1985) . The trig­ ger for sympatric speciation is the maintenance of genetic polymorphism in a spatially heterogeneous

population, where different genotypes are favoured in different patches . In such a system, selection can favour the evolution of preferential mating between like genotypes, thus preventing the production of segregant offspring that may be ill-adapted to all types of patch . The existence of races of phyo­ tophagous insect species that are adapted to dif­ ferent host species is often quoted as an example of sympatric speciation, but it is not clear whether these are examples of true species (Futuyma & Mayer 1980) . Since the theoretical conditions for the main­ tenance of genetic variation suitable for generating selection for preferential mating are rather severe (Seger 1985), the conclusion of Mayr (1963) that sympatric speciation is rare or non-existent seems likely to be essentially correct . A more promising alternative is parapatric specia­ tion, which involves the evolution of reproductive isolation between populations that are only par­ tially isolated geographically . The classic model of this process is that of Fisher (1930), who suggested that a set of populations distributed along a geo­ graphical gradient of selection pressure would ex­ perience selection for mating preferences that would reduce the flow of genes between populations, and hence prevent the introduction of genotypes that are ill-adapted to the local environment. Later theor­ etical work has confirmed that this is, indeed, a mechanistically plausible process (Endler 1977; Barton & Charlesworth 1984) . Of course, parapatric and allopatric speciation cannot be strictly dis­ tinguished, since populations at the extreme ends of a continental species range have very low prob­ abilities of exchanging genes. There are several classic examples of reproductive isolation between populations located at the ends of such species ranges which have bent round on themselves, so that the extremes are now in contact (Mayr 1963) . These represent cases in which reproductive iso­ lation has evolved between populations that are connected by a series of other, adjacent populations between which gene flow may well be possible . If the intermediate populations were to become ex­ tinct, such cases would be open to misinterpretation as examples of strict allopatric speciation . Further­ more, the fact that the degree of geographical iso­ lation tends to be correlated with divergence and speciation does not necessarily provide evidence for strict allopatric speciation, since (other things being equal) genetic divergence under the parapatric model will always be enhanced by restrictions on gene flow (Endler 1977) . While it is always possible to interpret phenomena such as hybrid zones and

2 . 2 Speciation geographically disjunct species ranges in terms of secondary contact between species that have di­ verged in allopatry, such interpretations are not necessarily demanded by the data . Thus, the biogeo­ graphical evidence does not seem to permit a clear­ cut conclusion to be drawn concerning whether or not speciation usually requires strict allopatry .

Ecological aspects of speciation Up to now, the ecological significance of speciation has not been mentioned . For two related species to coexist stably in the same area, it is necessary that they become adapted to somewhat different ecologi­ cal niches, otherwise the competitively superior one will cause the rapid extinction of the other . Especially in birds, there is extensive evidence for ecological differences between close relatives . The Galapagos finches provide a well documented example of the ecological divergence of related species, which appears to have been driven largely by divergent adaptations of geographically separ­ ated populations to different food sources (Grant 1986) . Without the evolution of such different ecol­ ogies, speciation would not result in any increase in biological diversity within a given geographical area . Sibling species show that such ecological dif­ ferences may arise without any gross morphological changes (Mayr 1963), although they are often associ­ ated with morphological differences, as in the case of the bills of the Galapagos finches . Ecological opportunities provided by the invasion of new habitats, unoccupied by competitors, must play a major role in stimulating the rapid increase in the number of species during adaptive radiations . Natu­ ral selection is, needless to say, the primary causal agent in this aspect of speciation (Grant 1986) .

Speciation and the fossil record Speciation, in the sense used here, is simply a population genetic process that results in the acqui­ sition of reproductive isolation between two for­ merly interbreeding populations. It thus cannot be directly observed in the fossil record . Indeed, it is important to recognize that, in a sense, there is no such thing as a speciation event, since all the evi­ dence suggests that the process of acquiring total reproductive isolation is a multistep process that requires numerous intermediate stages, examples of which can be studied in contemporary species (Mayr 1942, 1963) . Of course, the whole process of acquisition of specific status may occupy only a few

105

thousand generations, as witnessed by examples of good species that are nearly identical at the mol­ ecular level (Barton & Charlesworth 1984; Coyne & Orr 1989) . From the geological perspective, the time needed to develop complete reproductive isolation between two lineages may be effectively instan­ taneous . If no noticeable morphological differences evolve during the process, it will pass unnoticed in the fossil record, whereas morphological evolution in a single lineage might be counted as generating a new species, with the ancestral form A being re­ placed by a new form B. The fossil record thus provides a very incomplete picture of the process of speciation, particularly since subtle ecological, physiological and behavioural differences of the kind that frequently distinguish sibling species (Mayr 1963) will be missed . There are few cases in which it can be reasonably inferred that speciation has been observed in the record (Gingerich 1985; Section 2 . 3) . O f course, if form B appears in the record along­ side A, it may be reasonable to infer that B originated in a speciation event elsewhere, and subsequently migrated into the range of A, which is unchanged morphologically . Patterns of this kind have been well documented by Cheetham (1987), for example . This kind of observation is the basis for the claim often made by supporters of the theory of punctu­ ated equilibria, that morphological evolution usual­ ly only occurs in association with speciation (Gould & Eldredge 1977) . As Turner (1986) has shown, it does not necessarily provide firm evidence for this claim . If speciation is often unaccompanied by detectable morphological change, then a progenitor of B with the same morphology as A could have coexisted alongside A, and only be distinguished by the palaeontologist as a result of evolutionary change that occurred well after speciation . Provided that evolutionary change in morphology is episodic, as is to be expected on most models of adaptive evolution, the punctuational mode of evolution can be explained without ascribing a special causal relation between speciation and morphological change . Such a causal relation does not seem to be consistent either with the evidence from present day organisms, where morphological change un­ accompanied by reproductive isolation can be ob­ served (as in polytypic species), or with population genetic theory (Turner 1986) . Nevertheless, the association of speciation with geographical isolation, and with new ecological opportunities, means that a correlation between epi­ sodes of rapid speciation and morphological evol-

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2 The Evolutionary Process and the Fossil Record

ution and diversification is to be expected . Island radiations provide small-scale examples of this that have been intensively studied (Carson & Templeton 1984; Grant 1986) . Larger-scale events, such as the mammalian radiations of the Eocene, may be in­ ferred to have the same causes (Wright 1949), the successive occupation of new major modes of life by speciating lineages providing the basis for the origin of the diverse combinations of character­ istics distinguishing higher taxa (see also Section 3.6).

References Barton, N.H. & Charlesworth, B. 1984. Genetic revolutions, founder effects, and speciation. Annual Review of Ecology and Systematics 15, 133 - 1 64 . Carson, H.A. & Templeton, A.R. 1984 . Genetic revolutions in relation to speciation phenomena : the founding of new populations. Annual Review of Ecology and Systematics 15, 97- 131 . Cheetham, A . H . 1987. Tempo of evolution in a Neogene bryozoan: are trends in single morphologic characters misleading? Paleobiology 13 , 286-296. Coyne, J.A. & Orr, H . A . 1989. Patterns of speciation in Drosophila. Evolution 43, 362-381 . Darwin, C. 1 859 . The origin of species. John Murray, London. Dobzhansky, T. 1937. Genetics and the origin of species . Columbia University Press, New York. Endler, J.A. 1 977. Geographic variation, speciation and dines . Princeton University Press, New Jersey.

Fisher, R.A. 1930. The genetical theory of natural selection . Oxford University Press, Oxford . Futuyma, D . J . & Mayer, G . c . 1980. Non-allopatric speciation in animals . Systematic Zoology 29, 254- 271 . Gingerich, P . D . 1985 . Species in the fossil record: concepts, trends and transitions. Paleobiology 11, 27-41 . Gould, S.J. & Eldredge, N. 1977. Punctuated equilibria: the tempo and mode of evolution reconsidered . Paleobiology 3, 1 1 5 - 151 . Grant, P.R. 1986 . Ecology and evolution of Darwin's finches. Prince ton University Press, New Jersey. Mayr, E. 1942 . Systematics and the origin of species, p. 120. Columbia University Press, New York. Mayr, E. 1963. Animal species and evolution. Columbia University Press, New York. Muller, H.J. 1940 . Bearings of the Drosophila work on system­ atics. In: J . s . Huxley (ed . ) The new systematics, pp. 185 268 . Oxford University Press, Oxford. Seger, J. 1985 . Intraspecific resource competition as a cause of sympatric speciation. In: P.J. Greenwood, P . H . Harvey & M. Slatkin (eds) Evolution. Essays in honour of John Maynard Smith, pp . 43-54 . Cambridge University Press, Cambridge . Stebbins, G . L . 1950. Variation and evolution in plants . Columbia University Press, New York. Turner, J . R . G . 1986. The genetics of adaptive radiation: a neo-Darwinian view theory of punctuational evolution . I n : D . M . Raup & D . Jablonski (eds) Patterns and processes in the history of life, pp. 183-207. Springer-Verlag, Berlin. Wright, S. 1949 . Adaptation and selection. In: G . L . Jepsen, G . G . Simpson & E. Mayr (eds) Genetics, paleontology and evolution, pp. 365 -389 . Princeton University Press, New Jersey.

2 . 3 Microevolution and the Fossil Record P . R . SHELDON

Introduction Despite its many imperfections, the fossil record gives us a historical perspective on evolution that cannot be obtained from a study of living organisms alone . A lifetime' s research on, say, fruitflies in a laboratory or peppered moths in a wood, though indispensable, can only span a fleeting moment in a species' history. A crucial task for evolutionary biologists is to integrate results from an increasingly detailed analysis of the fossil record into a compre­ hensive synthetic theory, one which bridges the

gap between the neontological and palaeontological scales of observation . This explains the growing attention paid by geneticists to high-resolution fos­ sil data . The term microevolution is taken here to mean all the evolutionary changes that occur within a species up to and including the formation of new species, either by lineage branching (i. e . clado­ genesis or speciation) or by phyletic transformation (i. e . anagenesis) .

2 . 3 Microevolution Fossil species in practice Although the fossil record of any species will always be deficient vertically (in time), laterally (in space), and morphologically, the hard-part record of some forms - especially shelly marine invertebrates - is rather better than sometimes asserted. Attempts to quantify completeness of stratigraphic sections have enabled palaeontologists to calibrate accessible levels of time resolution, and to define the kinds of evolutionary and palaeoecological questions that the fossil record is uniquely placed to answer (Section 3. 1 2 ). The acquisition of reproductive isolation can never be directly observed in the fossil record (Section 2 . 2) . Nevertheless, many palaeontologists try to make the species they describe live up to a definition such as: 'Species are morphologically distinct groups within which variation is of the magnitude expected in interbreeding populations, and between which the differences are of the kind and degree expected to result from reproductive iso­ lation of natural populations'. In practice, of course, such species can never be more than 'morpho­ species' (units that embrace individuals of simi­ lar form), in which sibling species go undetected and from which truly con specific variants and sex­ ual dimorphs may be unwittingly excluded. Even greater conceptual problems arise if lineages under­ go extensive anagenesis : some workers, especially biostratigraphers, divide such lineages into arbit­ rary chronospecies, whilst others, mostly theorists adopting a strict cladistic approach, would prefer to denote a single unbranching lineage with a single specific name, irrespective of the total change. The more continuous the record, the more problematic the nomenclature (e. g. Bown & Rose 1987; Sheldon 1987).

Patterns of evolution The belief that many fossil species remained in mor­ phological stasis throughout their existence promp­ ted Eldredge and Could (1972) to invoke a pattern of punctuated equilibrium as an alternative to the pervasive paradigm of phyletic gradualism. Pre­ viously, lack of intermediates between species had largely been accounted for by incompleteness of the record. Basing their proposition on Mayr's al­ lopatric speciation model and on observations of Devonian trilobites and Pleistocene land snails, Eldredge and Could argued that the rise of new species is expected to be episodic, local, and rapid

1 07

(as opposed to continuous, widespread, and slow) and so the chance of finding intermediates in the fossil record is bound to be low. A speciation event would normally span less than 1% of the species' later existence in stasis. Fossil sequences should show stasis with sharp morphological breaks mark­ ing the migration of the descendant form from the peripheral, isolated area in which it developed. The presumed ancestor is then expected to persist for a while alongside its putative descendant. Thus, ac­ cording to punctuated equilibrium theory, signifi­ cant evolutionary change occurs at events of branching speciation and not during the in toto transformation of lineages. These contrasting pat­ terns have provided a very useful framework for discussion and stimulated a more rigorous analysis of the fossil record.

Perception of patterns It has often proved impossible to establish the validity of an evolutionary pattern to universal satisfaction. Many relevant hypotheses, such as ancestor - descendant relationships or genetic ver­ sus ecophenotypic change, are never truly verifiable. But here, as usual in palaeobiology, we are not in the business of proof but in assessing the relative probabilities of competing hypotheses. Fortey (1988) discussed the biases that influence perception of patterns, showing how it is com­ paratively easy for the convinced punctuationist to 'see' gradualistic change as a series of punctuation events. However, as intervals without data become restricted to smaller and smaller timespans, so one pattern rather than another can be shown to be more probable by applying the principle of parsi­ mony (though, of course, the most parsimonious explanation is not necessarily the correct one). Many of the standard textbook examples of gradu­ alism dissolved in the wake of the punctuated equi­ librium hypothesis. Most such cases were shown to lack sufficient documentation, whilst some, like the phylogeny of horses, were reinterpreted as showing punctuations, if anything. The ideal recipe for es­ tablishing evolutionary patterns includes some in­ gredients that are very difficult to obtain: many complete specimens from successive, small strati­ graphic intervals whose relative age is unequivocal; a framework of well-constrained absolute ages; samples spanning the entire geographical and tem­ poral range of all closely-related lineages; as many ontogenetic stages as possible (in order to recognize heterochronic relationships) and statistical data on

108

2 The Evolutionary Process and the Fossil Record

all available characters . To avoid generating artificial patterns, fossils should only be assigned to named species late in these procedures . A knowledge of geographical variation i s impor­ tant because spurious vertical patterns of phyletic change could arise in local sections by waves of immigration and emigration of intraspecific variants tracking their favoured environment. Also, in the­ ory, a peripheral isolate might evolve gradually to a new species which, on migration, appears abruptly alongside its parent species remaining in stasis . Geographical consistency of morphological change is not, however, a prerequisite for establishing the validity (i . e . genetic basis) of evolutionary trends . For example, dissimilar trends could occur i n adjac­ ent populations of a benthic species living in a tectonically unstable shelf area. The subpopulations might become isolated for a while in silled basins, each imposing different selection pressures, such as if one basin shallowed as another deepened . Eventu­ ally divergent strands of the lineage might be re­ united if the physical barriers to gene exchange were removed whilst hybridization was still possible .

Examples from the fossil record The case histories which follow have been selected to illustrate various aspects of the debate and for their implications for microevolutionary theory . Williamson (1981) presented evidence for both stasis and punctuated speciation in many lineages of Cenozoic lacustrine molluscs from East Africa. The 'speciation events', which took 5000 - 50 000 years, were accompanied by an increase in mor­ phological variance that Williamson interpreted as extreme developmental instability in transitional populations . The strong possibility remains, however, that the new short-lived forms were eco­ phenotypic variants induced by intense environ­ mental stress . Hallam (1982) concluded that the Jurassic oyster Gryphaea showed a step-like pattern of punctuated change, allied with morphological trends, some of which were paedomorphic . He found no evidence of gradualism or cladogenesis . Recently, however, Jonhson (in Fortey 1988) has reported gradual and continuous derivation of Gryphaea morphology in the Middle Jurassic from another oyster, Catinula . Stanley and Yang (1987) documented stasis in shape for 19 lineages of Neogene bivalves, some spanning as much as 17 million years without taxo­ nomically significant change . Populations millions of years old often resemble their Recent descend-

ants almost as closely as geographically separated conspecific living populations resemble each other. Stanley and Yang emphasized that shape and size should be kept separate in all calculations of evo­ lutionary rates, arguing that most reported trends relate to variables representing only some measure of body size . Cheetham (1987), examining 46 characteristics in nine species of Neogene bryozoans, found over­ whelming evidence for stasis and, by inference, punctuated speciation . The few within-species trends present related to features not used in species diagnoses and he cautioned against judging pat­ terns from single morphologic characters . Planktic foraminifera and radiolarians yield some of the best known lineages in the fossil record, because of their widespread distribution, abun­ dance in DSDP cores, and commercial use in bio­ stratigraphy . These micro-organisms display a wide variety of evolutionary tempos and modes (see papers in Paleobiology 9 (4), 1 983, and Banner & Lowry in Cope & Skelton 1985 for reviews) . Gradual changes seem relatively common. Malmgren and Kennett (1981) demonstrated persistent gradualism in a lineage of temperate foraminifera that spanned four successive chronospecies in 8 million years . Planktic foraminifera also show a pattern best de­ scribed as punctuated anagenesis (e . g . Malmgren et al. 1983), which is probably common in other groups too, including ammonites (e . g . Callomon in Cope & Skelton 1985) . Sheldon (1987) reported parallel gradualistic evo­ lution of benthic Ordovician trilobites from central Wales . Over a period of c. 3 million years eight lineages underwent a net increase in the number of pygidial ribs, a character used in species diagnosis (Fig. 1 ) . The end members of most lineages had previously been assigned to different species and, in one case, to different genera . In view of inter­ mediate morphologies and temporary trend rever­ sals, practical taxonomic subdivision of each lineage proved impossible . The apparent success of earlier Linnean nomenclature (with its implications of dis­ crete species) could easily have been misinterpreted as evidence of punctuation and stasis . Perception of many other gradualistic patterns equally may have been hindered by conventional descriptive procedures, particularly the requirement to apply binominal taxonomy to fossils and the practice of lumping together specimens collected from different horizons in order to amass enough material for full 'species' description . Although vertebrate data are sparse, gradual evo-

2 .3 Microevolution

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lution appears to be fairly common, particularly in Tertiary mammals (e . g . Gingerich 1985; Godinot in Cope & Skelton 1985) . Bown & Rose (1987) saw no sign of stasis in Eocene primates from Wyoming, reporting both gradual anagenesis and cladogenesis in sharp contradiction to the predictions of the punctuated equilibrium model . They highlighted the problems that gradualism causes for systematic palaeontology and biostratigraphy . Bell et al. (1985), in a multicharacter study of a Miocene stickleback lineage, found that taxonomically significant mor­ phological change was accomplished by protracted trends and by rapid bursts of evolution, without tight synchrony of change among characters (mosaic evolution) . Although there are some well attested examples of gradual cladogenesis in the fossil record (Gingerich 1985), the great rarity of branching points where nodes are known is consistent with common patterns of change in which cladogenesis is rapid and/or involves small, isolated populations .

Random change and trend reversals There has been much interest in the possibility that some morphological trends seen in the fossil record may be the result of processes other than natural selection . The genetic drift hypothesis predicts that

the morphology of selectively-neutral characters will vary through time as a random walk. Indeed, it has been argued that evolutionary rates exist only when the hypothesis of a symmetrical random walk can be refuted . However, Sheldon (1987) argued that temporary reversals of variable characters probably occur in all evolutionary lineages, and so many trends driven by selection may be indistinguishable from random walks . Reversals probably reflect times when some other attribute, genetically uncorrelated with the one under consideration, was selected . It would be unreasonable to expect that the one feature chosen for plotting was consistently the only one favoured by selection, or that it was always linked to every other favoured trait . In fact, long-sustained net trends in a single character may reflect genetic coupling to other characters having negative effects on fitness (see also Section 2 .2) . The widespread tendency not to expect reversals, or to interpret them as ecophenotypic change or random drift, led to the unrealistic portrayal of phyletic gradualism as unidirectional change . Re­ versals have many consequences . For instance, they complicate the theoretical arguments (Fortey 1988) concerning differentiation between cases of gradu­ alism and punctuated equilibria; they should not be automatically taken to indicate that the observed change is only ecophenotypic; and jumps in mor-

110

2 The Evolutionary Process and the Fossil Record

phological trends cannot be used to estimate the amount of time missing at diastems .

Patterns of evolution in different environments It is still inappropriate to estimate the relative im­ portance of particular patterns of evolution in dif­ ferent environments . Given the immense range of attributes of living organisms (e . g . complex life cycles and reproductive strategies) it would not be surprising to find different patterns emerging from broadly similar environments . Benthic inver­ tebrates, for instance, have a wide diversity of larval dispersal modes and these early stages, although rarely preserved, might profoundly influence pat­ terns . There is some evidence, as might be expected, that abrupt speciation and extinction are commonly associated with benthic species living in shallow marine settings . However, Sheldon (1987) suggested that, almost paradoxically, stasis seems to prevail in these more widely fluctuating, rapidly changing environments, whereas species living in, or able to track, narrowly fluctuating, slowly changing environments show persistent phyletic evolution rather than stasis . Some of the perceived punctuations in shallow benthic settings may simply reflect higher rates of short-term deposition and more hiatuses (less completeness) than in offshore, pelagic environ­ ments . But, although the most reliable evolution­ ary patterns will come from the most complete sequences, the depositional conditions promoting completeness might in themselves encourage grad­ ual phyletic evolution, especially of benthos.

Conclusion Studies of the fossil record have revealed a wide spectrum of microevolutionary patterns, from which can be inferred a variety of evolutionary processes. Punctuated equilibrium and phyletic gradualism should be viewed as just two theoretical versions of many possible evolutionary patterns and the temp­ tation to force poorly documented cases to fit one or other of these models must be resisted . Often there is simply too little data to assess patterns of change as, for example, with the genus Homo (Section 1 . 12) . We are not yet in a position to assess accurately the relative frequency of particular patterns and the domain of their expected settings .

Individual taxa probably exhibit different pat­ terns at different times, and different morphological characters in the same species may evolve at differ­ ent rates . Episodic changes need not be associated with branching events and demonstrating stasis in a species is not the same as demonstrating punctu­ ated speciation . Most geneticists believe that a punctuated appear­ ance of species is consistent with neo-Darwinian theory . In many ways it is explaining stasis which is certainly more prevalent than would have been predicted from studies of living organisms that represents the greater challenge .

References Bell, M . A . , Baumgartner, J.V. & Olson, E . c . 1985 . Patterns of temporal change in single morphological characters of a Miocene stickleback fish. Paleobiology 11, 258 -271 . Bown, T.M & Rose, K.D. 1987. Patterns of dental evolution in early Eocene anaptomorphine primates (Omomyidae) from the Bighorn Basin, Wyoming. Memoir of the Paleontological Society 23, 162 pp. Cheetham, A.H. 1987. Tempo of evolution in a Neogene bryozoan: are trends in single morphologic characters misleading? Paleobiology 13, 286-296 . Cope, J . C .W. & Skeiton, P.W. (eds) 1985 . Evolutionary case histories from the fossil record . Special Papers in Palae­ ontology 33, 1 - 203. Eldredge, N . & Could, S.J. 1972. Punctuated equilibria; an alternative to phyletic gradualism. In: T.J.M. Schopf (ed .) Models in paleobiology, pp. 82 - 1 15. Freeman, San Francisco . Fortey, R.A. 1988. Seeing is believing: gradualism and punc­ tuated equilibria in the fossil record . Science Progress 72, 1 - 19 . Cingerich, P.D. 1985 . Species i n the fossil record : concepts, trends, and transitions . Paleobiology 11, 27-41 . Hallam, A. 1982. Patterns of speciation in Jurassic Gryphaea. Paleobiology 8, 354-366 . Malmgren, B . A . & Kennett, J . P . 1981 . Phyletic gradualism in a Late Cenozoic planktonic foraminiferal lineage; DSDP Site 284, southwest Pacific. Paleobiology 7, 230-240. Malmgren, B . A . , Berggren, W.A. & Lohmann, C . P . 1983. Evidence for punctuated gradualism in the Late Neogene Globorotalia tumida lineage of planktonic foraminifera. Paleobiology 9, 377-389 . Sheldon, P.R. 1987. Parallel gradualistic evolution of Ordovician trilobites. Nature 330, 561 -563. Stanley, S . M . & Yang, X. 1987. Approximate evolutionary stasis for bivalve morphology over millions of years: a multivariate, multilineage study. Paleobiology 13, 1 1 3 - 139. Williamson, P.C. 1981 . Palaeontological documentation of speciation in Cenozoic molluscs from Turkana Basin. Nature 293, 437- 443.

2.4 Heterochrony K . J . McNAMARA

Introduction Heterochrony is the phenomenon of changes through time in the appearance or rate of develop­ ment of ancestral characters . While the recognition of a close relationship between ontogeny and phylo­ geny has a long history it was not until the late nineteenth century that it was formalized by E . Haeckel i n his 'Biogenetic Law' (ontogeny recapitu­ lates phylogeny) . This involved a change in the timing of developmental events; but only in one direction - by terminal addition . Phylogenetically this meant that ancestral adult forms were encapsu­ lated in the juvenile stages of their descendants . This became known as recapitulation . Exceptions to this rule (known as 'degenerate' forms) were noted by the leading protagonists of recapitulation, particularly palaeontologists such as A. Hyatt (ammonites), R. Jackson (echinoids and bivalves), and C . E . Beecher (trilobites and brachio­ pods) . With the awareness that these so-called de­ generate forms were at least as common as examples of recapitulation, the Biogenetic Law began to slide into oblivion . I n the nineteen-twenties W. Garstang recognized that ontogeny did not always recapitulate phy­ logeny - it created it. Garstang believed that the retention of ancestral juvenile characters by de­ scendant adults, which he termed paedomorphosis, was the key to understanding the evolution of many major groups of organisms, in particular the evol­ ution of vertebrates from tunicate larvae . However, recent research has shown that both paedomor­ phosis and 'recapitulation' play important roles in evolution (Gould 1977; Alberch et al. 1 979; McNamara 1986a; McKinney & McNamara 199 1 ) .

the timing of onset or cessation of morphological development and size change can also produce heterochrony . If size alone changes between ances­ tor and descendant, dwarfs or giants are produced. If the rate of shape change is increased, or its period of operation is extended, the descendant adult passes morphologically 'beyond' the ancestor: this is peramorphosis (this equates, to some degree, with the Haekelian 'recapitulation') . Conversely, if the rate of shape change is reduced, or its period of operation is contracted, the descendant adult passes through fewer growth stages, so resembling a juven­ ile stage of the ancestor: this is paedomorphosis . These terms can be applied not only to the appear­ ance of meristic characters (in other words, individ­ ual structures produced during an organism' s ontogeny) but also to subsequent changes of shape of these structures during ontogeny . Thus not only may the rate of induction of structures vary, but the structures which are produced may show phylo­ genetic changes as they vary their rate of shape change . These two basic forms of heterochrony are known respectively as differentiative heterochrony and growth heterochrony (Figs 1, 2) . The relationship between size and shape is known as allometry. If the relative size and shape of a structure remain the same relative to overall body size during ontogeny, growth is isometric. However, if a particular structure increases in size relative to the whole organism, as well as changing its shape, growth shows positive allometry. Should a structure decrease in relative size, growth shows negative allometry. Increasing the degree of allometry is expressed phylogenetically as peramorphosis . Reducing it produces paedomorphosis . Similarly, extending or contracting the period of allometric growth produces peramorphic or paedomorphic descendants respectively . Paedomorphosis and peramorphosis are morpho­ logical expressions of heterochronic processes. Pae­ domorphosis can occur by progenesis, neoteny, or post-displacement (Fig . 1) . Peramorphosis can occur by hypermorphosis, acceleration, or pre-displacement (Fig. 2) .

Nomenclature Heterochrony involves the decoupling of the three fundamental elements of growth: size, shape, and time, or the extension or contraction of these el­ ements . Temporal changes of size and shape relative to one another produce heterochrony, when either size or shape, or both, are affected by changes in their rate of ontogenetic development . Changes to

111

2 The Evolutionary Process and the Fossil Record

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Progenesis often occurs by precocious sexual maturation . Consequently morphological and size development is prematurely stopped, or severely retarded . The resultant adult paedomorph will be smaller than the ancestral adult . The prematuration morphological history of both the progenetic form and its ancestor will be identical . Progenesis is often global, affecting all structures, but it may also affect local growth fields . Some characters, how­ ever, are likely to have a more distinctly juvenile appearance than others . Thus, in the fossil record, it is generally possible to deduce the operation of progenesis : the morphotype is smaller than its presumed ancestor and resembles a juvenile stage of the ancestor. It will, however, be appreciably larger than the corresponding ancestral juvenile stage .

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onset of growth of particular morphological struc­ tures . Thus, by comparison with the ancestor, a structure commences development at a later stage, compared with other parts of the organism . Should subsequent development and cessation of growth be the same in the descendant as in the ancestor, the displaced structure will attain a shape at maturity resembling that found in a juvenile of the ancestral form. The displaced structure is also likely to be smaller than in the ancestor .

Hypermorphosis occurs by extending the juvenile 1 The relationship of the three paedomorphic processes to the ancestor. Progenesis occurs by precocious maturation, post-displacement by the delayed onset of growth, and neoteny by reduced rate of morphological development. Differentiative paedomorphosis is shown by the spine production, growth paedomorphosis by the central spot. (From McNamara 1986a . ) Fig.

growth period, by a delay in the onset of sexual maturation . Early juvenile development will progress at the same rate as in the ancestor. By extending growth allometries to a larger size, the hypermorphic adult can attain morphological charac­ teristics quite distinct from those of the ancestral adult . Like progenesis, hypermorphosis is often global in its effects, but it too can affect only local growth fields .

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Pre-displacement involves the earlier onset of growth of a specific structure . This allows a longer period of growth and development . Ancestral allometries will therefore, in effect, be extended . The resultant struc­ ture will be more advanced morphologically and larger than the equivalent structure in the ancestral adult, so long as cessation and rate of growth are identical in ancestor and descendant .

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The identification of heterochronic processes in the fossil record is generally based on the precept that these processes can be characterized by the study of size and shape alone . The assumption is made that size is a proxy for time : the larger the organism, the longer period of time it took to reach that size. This assumption may not always be valid . She a (1983) has suggested that two forms of pro­ genesis and hypermorphosis can be recognized . In the first, time and size are not dissociated; thus smaller size correlates with shorter time, larger size with longer time . This Shea calls 'time hypomor­ phosis ( progenesis)' . The corresponding pera­ morphic process is time hypermorphosis . In the second case the progenetic form attained its reduced size and shape in the same amount of time that the ancestor took to attain maturity. This occurred because the rates of size and shape change were equally reduced through ontogeny compared with the ancestor . This Shea termed 'rate hypomorphosis ( progenesis)' . Time and rate progenesis or hyper­ morphosis can theoretically be distinguished in the fossil record . Early ancestral and descendant onto­ genies will be the same when time progenesis has occurred, whereas they will differ in rate progenesis . Future emphasis on the study of growth lines in suitable invertebrate groups, such as molluscs, corals, and echinoids, will allow the true rates of growth of fossil organisms to be ascertained (McKinney 1988) . =

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Fig. 2 The relationship of the three peramorphic processes to the ancestor . Hypermorphosis occurs by delayed sexual maturation, pre-displacement by earlier onset of growth, and acceleration by increasing the rate of morphological development. The spines and central spot demonstrate differentiative and mitotic peramorphosis, respectively. (From McNamara 1986a . )

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2 The Evolutionary Process and the Fossil Record

Heterochrony at different hierarchical levels While most of the literature dealing with hetero­ chrony as a factor in evolution concentrates on its role at the specific or supraspecific level, it needs to be stressed that much recognized intraspecific morphological variation in populations is, in fact, engendered by heterochronic processes . These act upon both meristic and allometric traits . For instance, intraspecific variation in ammonites often involves variation in the numbers of ribs or tuber­ cles generated at a certain size . Similarly, in echinoids intraspecific variation often involves dif­ ferences in the rate of production of meristic charac­ ters, such as the number of coronal plates and spines . Variation in numbers of these structures between two individuals of the same size may be accounted for either by variations in rates of devel­ opment (neoteny or acceleration) or by onset and offset of growth (pre- or post-displacement and progenesis or hypermorphosis) . However, variations in rate of size increase may also produce such intraspecific differences . Thus if two individuals from a single population each 20 mm in length possess, in one case, six spines, and in the other eight, this may reflect a variation in rate of spine development (neoteny or acceleration), if both attained 20 mm in the same period of time . Alternatively, the individual with six spines may have increased in size at a faster rate through onto­ geny, and thus only have had sufficient time to generate six spines . It is possible to test whether this latter mechanism has occurred by analysing the developmental patterns of other structures . For instance, if one of these organisms reached a length of 20 mm faster than the other, then all of its structures should appear relatively paedomorphic. However if, as is often the case, intrapopulational variation shows some characters to be paedomor­ phic and others peramorphic, then rates of structural development will have changed . Selection o f heterochronic morphotypes, and the resultant morphological evolution of a new species, is reflected in substantial shifts in the mean values of heritable phenotypic variation of shape or size of morphological structures . These occur by pertur­ bations to the developmental programme . These may be under strong directional selection pressure (see below) . Evolution of a substantial new hetero­ chronic morphology may result in the evolution of new adaptive structures . These allow either geo­ graphical or ecological separation from the ancestral stock, and subsequent genetic isolation and estab-

lishment of a new species (see also Section 2 . 2) . In recent years documentation of heterochrony in the fossil record at the interspecific level has been undertaken in particular on ammonites (see McKinney 1988), echinoids (McNamara 1988), and trilobites (McNamara 1986b) . It has been suggested (McNamara 1982) that heterochrony may be one of the factors responsible for rapid speciation events. This is particularly so where progenesis or hyper­ morphosis have occurred . However, gradual, phy­ letic changes may equally well be engendered by small modifications in growth rates between popu­ lations, resulting in subtle shifts in morphology through time. Heterochrony has been proposed as a major factor in evolution at the supraspecific level . For instance, the orthodox view of the origin of vertebrates is that they may have arisen from the pelagic larva of a tunicate-like deuterostome invertebrate . This would have occurred by progenesis from an early larval stage . The free-swimming tunicate larva possesses all the fundamental chordate characters : a noto­ chord, dorsal hollow nerve cord, gill slits, and post­ anal propulsive tail. Attainment of precocious sexual maturation would have caused the retention of such ancestral larval characters into the adult phase and a consequent major adaptive breakthrough . The earlier that perturbations to the embryo­ logical developmental system occur, the more profound the morphological consequence . Taxo­ nomically, this is likely to be expressed at a high level. For instance, it has been suggested (McNamara in McKinney 1988) that progenesis at early developmental stages has been instrumental in the evolution of a number of higher taxa: saleniid, tiarechinid, neolampadoid, and clypeasteroid echinoids; edrioasteroids; baculitid ammonites; thecideidine and craniacean brachiopods; and branchiosaurid amphibians (Fig. 3) . Other heterochronic processes have also been instrumental in the evolution of higher taxa . For instance, it has been proposed that birds may have evolved from theropod dinosaurs . The very large orbits of birds, their inflated braincase, retarded dental development, and overall limb proportions indicate that early birds may have been paedomor­ phic theropods. Feathers are thought to have been present on juvenile theropods . The paedomorphic processes were probably neoteny and post­ displacement .

2 . 4 Heterochrony

115

include the evolution of a number of anagenetic paedo- and peramorphoclines in spatangoid echin­ oids, such as Schizaster, Hemiaster, Lovenia, Pericosmus, and Protenaster (Fig. 4) . All show evolution from coarse to fine-grained sediments (probably shallow to deep water) . Conversely, the Cenozoic brachiopod Tegulorhynchia evolved along a paedomorphocline from deep to shallow water into the genus Notosaria (Fig . 5) . Similarly a number of trilobite lineages are thought to have evolved by heterochrony along the same environmental gradient (McNamara 1986b) . In the marine environment changing water depth and sediment type are frequent environ­ mental gradients along which paedo- and peramor­ phoclines develop .

Ecological causation of heterochrony

Fig. 3

Reconstruction o f a paedomorphic branchiosaurid amphibian.

Heterochrony and directed speciation The pattern that is emerging from studies of hetero­ chrony in the fossil record is one of frequent directed heterochronic speciation . The direction of morpho­ logical evolution is strongly constrained by the nature of the organism's own ontogeny. Thus a number of characters in a lineage may show progressive paedomorphosis or peramorphosis . Provided that the descendant morphotypes are suitably adapted along an environmental gradient, a phylogenetic trend, in the form of a paedomorpho­ dine or peramorphodine, may develop . The environ­ mental and morphological directionality may be induced by the effects of either competition or predation. With induction of the heterochronic morphological gradient by competition, the persist­ ence of the ancestral form constrains selection to one direction: along the environmental gradient away from the ancestral species . The phylogenetic pattern generated will be one of cladogenesis . Selec­ tive pressure from predation in one environment may induce the evolution of a paedo- or peramor­ phocline . In this case the phylogenetic pattern is one of anagenetic speciation . Recent studies of echinoids, brachiopods, bi­ valves, ammonites, graptolites, and ammonites (see McNamara in McKinney 1988) indicate that the anagenetic pattern is common . Specific examples

While many of the examples of directed hetero­ chronic evolution have been interpreted as having arisen by selection of morphologically adaptive characters, it has also been argued that other factors, such as life history strategies, which affect elements such as size and time of maturation, may also be targets of selection. McKinney (1986) has suggested that for a suite of Tertiary echinoids selection favoured large forms along an environmental gradi­ ent from shallow to deep water (equating with unstable to stable environments) (Fig. 6) . He argued that any subsequent morphological changes were incidental allometric by-products of the size change . The larger size was attained either by slower, neo­ tenic growth or by extended, hypermorphic growth . This indicates that the target of selection was repro­ ductive timing and/or body size . Such size increase along lineages (Cope's Rule; Section 2 . 10) may reflect K-selective pressure (large body size, delayed reproduction and development, and longer life spans in a stable environment) . While analyses of other echinoid lineages does not provide unequivocal corroboration of this pattern, there is ample evidence that many pro­ genetic species are, conversely, r-selected (small body size, early maturation, high fecundity, and short life span in an unstable environment) . Many so-called 'dwarfed' faunas may be r-strategists, inhabiting unstable, fluctuating environments . The small body size of progenetic Late Cretaceous oys­ ters and ammonites may have been an adaptation to a soft, unstable substrate . The same is true for many progenetic brachiopods . High fecundity of progenetic species has been documented in edrioas­ teroids and trilobites (McNamara in McKinney

2 The Evolutionary Process and the Fossil Record

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1988) . Although in these cases small size and pre­ cocious maturation may have been the principal targets of selection, unless the resultant progenetic morphology was also adaptively significant in the new environment, selection would not have occurred . Most heterochronic changes occur a s a result of changes to the internal developmental regulatory system. However, certain changes may actually be induced by environmental perturbations . The effect of changing environmental pressures may lead to facultative heterochrony within populations . For instance, the frequency of development of pae­ domorphs in living populations of salamanders is directly influenced by the population density . When low, a large proportion of individuals develop as neotenic paedomorphs, attaining maturity in their larval form, so remaining and reproducing in the aquatic environment . At high population densities

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few individuals are paedomorphic, the high density levels inducing metamorphosis to the terrestrial form . There is also indirect evidence from the fossil record (McNamara 1986b) that changes in water temperature at different water depths in the marine environment may have been a factor in inducing progenesis in a number of lineages of Cambrian trilobites . Experimental work has demonstrated the effect of higher temperatures in inducing premature maturation in some living arthropods .

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Frequency of heterochrony in the fossil record Any attempt to assess the frequency of heterochrony or of the heterochronic processes is fraught with problems, not the least of which are historical prejudices . While the Haeckelian school were blink­ ered to the existence of paedomorphosis, the Garstang/de Beer school were equally contemptuous of peramorphosis . In a recent survey of palaeon­ tological literature from 1976 to 1985, McNamara (in McKinney 1988) documented 272 examples of heterochrony; of these, 179 were of paedomorphosis, the remaining 93 were of peramorphosis . The most comprehensive recent analyses of heterochrony in the fossil record have centred on trilobites, echinoids, ammonites, bryozoans, and graptolites . These studies have shown both pae­ domorphosis and peramorphosis to be important factors, but paedomorphosis still predominates . The greater frequency of paedomorphosis, if true, may occur because existing developmental programmes are utilized . Peramorphosis always requires the pro­ duction of novel bauplans by extending the pre­ existing developmental pathways . Trilobites show a changing relative frequency of paedomorphosis and peramorphosis . During the Cambrian paedomorphosis, particularly that in­ duced by progenesis, was predominant . Post­ Cambrian forms, however, show a marked decline in the incidence of progenesis and a greater fre­ quency of peramorphosis . It has been argued (McNamara 1986b) that this change may reflect an improvement in regulation of the developmental system in later trilobites .

117

Recent analysis of heterochrony in irregular echinoids (McNamara 1988) has highlighted the complex activity of heterochrony in single lineages, some characters being paedomorphic, others pera­ morphic. Furthermore, one paedomorphic structure might have evolved by neoteny, whilst another might have formed by post-displacement . The operation of a complex array of heterochronic pro­ cesses has been termed mosaic heterochrony. With each structural element of an organism essentially following its own ontogenetic trajectory, and each being potentially subject to changes in develop­ mental regulation, there is the possibility of the evolution of a multitude of heterochronic morpho­ types . Any one of these may potentially form a new species, with the target of selection being the result­ ant morphotypes, size, or life history strategies . Ammonites have featured prominently in studies of heterochrony for over 100 years . They were used initially as examples of 'recapitulation' , by Hyatt and co-workers; while to O. Schindewolf and other workers in the first half of this century they showed evidence only of paedomorphosis . Recent research (see McKinney 1988) has shown the ubiquity of both phenomena, but peramorphosis, particularly of the septa, appears more common than paedomor­ phosis . Colonial organisms, such as bryozoans and grap­ tolites, sJ;tow a two-tiered heterochronic pattern . Both the individual animals and the colony as a whole may be affected by heterochrony . The former is known as ontogenetic heterochrony, the latter as astogenetic heterochrony. This two-tiered structure is comparable with the two-tiered structure of dif­ fentiative and mitotic heterochrony present in non­ colonial organisms . Astogenetic heterochrony has been reported more often than ontogenetic hetero­ chrony (McKinney 1988), perhaps because astoge­ ne tic changes reflect developmental modification of ontogenetic characters, so reflecting the individuality of the colony as a whole . Heterochrony in colonial organisms may have been important in macroevo­ lution . Ontogenetic heterochrony in highly inte­ grated colonies may result in large morphological differences between ancestor and descendant . It would appear that periods of reef building cor­ respond to periods of high integration in colonial animals . It is likely, therefore, that astogenetic heterochrony will predominate during periods of reef building . Many of the examples of heterochrony involving vertebrates occur in amphibians . Most of these show paedomorphosis, akin to that seen in living

118

2 The Evolutionary Process and the Fossil Record

salamanders . Many of the interspecific and inter­ generic differences in allometry of skull plates in Palaeozoic fishes are the result of mitotic hetero­ chrony, though few studies have actually couched it in these terms . Similarly, phylogenetic changes in limb allometries in mammals are due to hetero­ chrony . The limited evidence from studies of mammals seems to suggest a predominance of peramorphosis over paedomorphosis . This may occur because of the frequent operation of Cope's Rule in mammal lineages, suggesting size as being an important target of selection . For example, exten­ sion of ancestral allometries by increased size in horses through the Tertiary resulted in peramorphic descendants by hypermorphosis . However, some characters, such as development of the foot, show paedomorphic reduction in some digits .

Developmental processes underlying heterochrony Changes to the onset, offset and rate of growth of morphological characters are essentially under three interactive levels of control: genetic, hormonal, and cellular. Perturbations to the genetic regulation of hormonal and cellular development, particularly at early embryological stages, are likely to be critical factors in heterochrony . Developmental regulation is not simply a matter of discrete entities called 'regulatory genes' acting upon 'structural genes' . It involves a complex inter­ action between active sites or structural components of proteins, combined with cell - cell interactions (Campbell & Day 1987) . Developmental processes are controlled by highly organized, dynamically structured multigene families . The manner in which the genome is encoded and expressed in develop­ ment is far from clear, although it would seem that only a small area of the highly dynamic, constantly changing genome is occupied by genes for development . The region involved in regulation in a typical eukaryote gene is the promotor region . This contains DNA binding proteins specific to the gene, and capable of controlling the level of transcription . The role of the promoter sequence in gene control, and its effect on growth, highlights the activity of hor­ mones in growth, and how perturbations to the genetic control of hormone production can have a strong phenotypic expression . Growth, moulting, and sexual reproduction in arthropods, for instance, are all under hormonal control. It has been suggested (Campbell & Day

1987) that hexapods evolved from a myriapodous ancestor by progenesis : a small change in the genetic control of the hormone responsible for the incep­ tion of maturation, and of the hormone controlling post-larval development, had a profound effect on the phenotype . Even within fossil lineages the activity of genes controlling hormone production can be inferred . Two forms of progenesis in trilo­ bites have been identified : sequential and terminal (McNamara 1986b) . Terminal progenesis is likely to have occurred by a premature cessation in pro­ duction of a juvenile hormone . Sequential pro­ genesis, where each intermoult period is shortened, is thought to have occurred by premature pro­ duction of an ecdysone-like moulting hormone during each intermoult period. This premature hormonal activity will have been under direct genetic control . The third factor in the developmental processes that cause heterochrony is activity at the cellular level . Hall (1984) has stressed the importance of the number and mitotic activity of the cells in the initial skeletal condensation in vertebrates . Thus onset of growth is determined by the number of stem cells that start condensation, the proportion that divides, rate of cell division, and amount of cell death . These parameters all act early in development and deter­ mine the time of onset of growth . The rate of growth of skeletal elements is influenced by adjacent tissues, hormones, and allometric factors . Muscle action, tendon insertion, blood flow, innervation, and growth of adjacent tissues modulate the growth rate . Cessation of growth is partially determined very early in development by the number of growth plate cells and the number of times they divide . Timing of development of secondary ossification centres also affects the offset signal . Metabolic inhibition by production of a growth inhibitor to suppress cell proliferation and protein synthesis also stops growth .

References Alberch, P., Could, S .J . , Oster, C . F . & Wake, D . B . 1979 . Size and shape in ontogeny and phylogeny. Paleobiology 5, 296 -317. Campbell, K.S.W. & Day, M . F . (eds) 1987. Rates of evolution . AlIen & Unwin, London. Could, S.J. 1977. Ontogeny and phylogeny. Belknap Press, Cambridge . Hall, B . K . 1984. Developmental processes underlying hetero­ chrony as an evolutionary mechanism. Canadian Journal of Zoology 62, 1 - 7. McKinney, M.L. 1986. Ecological causation of heterochrony:

2 . 5 Red Queen Hypothesis test and implications for evolutionary theory. Paleobiology 12, 282 -289 . McKinney, M . L . (ed . ) 1988. Heterochrony in evolution: a multi­ disciplinary approach . Plenum Press, New York. McKinney, M . L . & McNamara, K.J. 1991 . Heterochrony: the evolution of ontogeny. Plenum Press, New York. McNamara, K.J. 1982 . Heterochrony and phylogenetic trends. Paleobiology 8, 130 - 142 . McNamara, K . J . 1983 . The earliest Tegulorhynchia (Brachio­ poda : Rhynconellida) and its evolutionary significance. Journal of Paleontology 57, 461 -473 . McNamara, K.J. 1985 . Taxonomy and evolution of the Caino­ zoic spatangoid echinoid Protenaster. Palaeontology 28,

119

31 1 - 330 . McNamara, K.J. 1986a. A guide to the nomenclature of hetero­ chrony. Journal of Paleontology 60, 4 - 1 3 . McNamara, K.J. 1986b . The role o f heterochrony i n the evol­ ution of Cambrian trilobites . Biological Reviews 6 1 , 121 - 156 . McNamara, K . J . 1988 . Heterochrony and the evolution of echinoids. In: e . R . e . Paul & A . B . Smith (eds) Echinoderm phylogeny and evolutionary biology. Oxford University Press, Oxford . Shea, B.T. 1983. Allometry and heterochrony in the African apes . American Journal of Physical Anthropology 62, 275 - 289 .

2 . 5 Red Queen Hypothesis M . J . BENTON

Introduction Palaeontologists have long argued that the distinc­ tive features of the evolution of life were produced by changes in the physical environment. Changes in climate, or in sea-level, for instance, might explain why certain groups died out, or why an adaptive radiation took place at a particular time . This trend has continued in recent research into mass extinc­ tions (Section 2 . 12), whether their cause is said to be changes in the earthbound physical environ­ ment, or the impact of asteroids . O n the other hand, many ecologists have viewed the large-scale aspects of evolution (macroevolution) as simply a scaled-up version of microevolution . Evolutionary change, they argue, can be produced by competition between organisms, and by inter­ actions between predators and prey . This ecological view stresses the influence of the biotic environ­ ment, that is, other plants and animals, on evolution .

Van Valen's Law The ecological view of macroevolution was codified by Van Valen (1973), who presented palaeontologi­ cal and ecological evidence for a model of evolution that depended on the biotic environment, and termed the model the Red Queen Hypothesis . The palaeontological evidence was based on a study of

the rates at which different groups of plants and animals go extinct through time . Van Valen used plots of species survivorship (Fig. 1) which showed the proportions of an original sample of organisms that survive for various intervals . He found, contrary to his expectations, that the probability of extinction within any group remained constant through time - his Law of Constant Extinction. For example, families or species of modern mammals are just as likely to become extinct as were their Mesozoic ancestors living 200 Ma. A species might disappear at any time, irrespective of how long it has already existed . Evolutionary biologists might have intuit­ ively expected species within any group to become longer-lived over time on average . Van Valen's start­ ling discovery seemed to deny some basic assump­ tions of evolution . If evolution is taken to mean improvement in the adaptation of a species to its environment through time, why is it that modern mammals are not better at surviving than their Mesozoic forebears? Van Valen's explanation for the Law of Constant Extinction was that the various species within a community maintain constant ecological relation­ ships relative to each other, and that these inter­ actions are themselves evolving . Thus, the antelope on an African savanna, for example, evolves greater speed in order to escape from the lion, but the lion

120

2 The Evolutionary Process and the Fossil Record

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also evolves greater speed in order to catch its dinner. The status quo is maintained . If biotic inter­ actions did not follow a pattern of ever-moving dynamic equilibrium, the community would be shattered . Were all antelopes to achieve a quantum improvement in their running speed, lions would starve and populations of antelope might outstrip the carrying capacity of the environment. This balance is the Red Queen Hypothesis. [In Lewis Carroll's Through the Looking Glass, the Red Queen told Alice, 'Now here, you see, it takes all the running you can do, to keep in the same place' . ] After 1 973, many biologists accepted the Red Queen model, while others were critical . The main problem was simply the counter-intuitive claim that species do not improve their chances of survival through time . If organisms are continuously evol­ ving and adapting, why do they not get any better, on average, at avoiding extinction? There were prob­ lems also with Van Valen' s particular formulation of the Red Queen model . He explicitly made a zero­ sum assumption : that there were fixed amounts of energy available to communities, and that any gain by one species was exactly offset by equal losses to others . It is not at all clear, however, that the amounts of energy, or resources in general, have remained constant through time . It is equally prob­ able that the total global biomass has increased markedly many times as major new habitats were exploited (e . g . the move onto land (Section 1 . 8), the evolution of 'trees', the origin of flight (Section 1 . 9), and the evolution of deep-burrowing habits by various marine groups (Section 1 . 7. 1 ) ) . The increase in biomass is possible by pulling more of the global carbon into the biotic part of the biogeochemical cycle, and/or by speeding up the rate at which carbon, and other essential elements, are cycled through the system (Benton 1987) .

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Problems with 'progress', and the Stationary Model Although the Red Queen model does not predict improvements in the ability to avoid extinction, it does explicitly assume that, within any lineage, later members will be competitively superior to earlier ones: that a present-day antelope can run faster than its Pliocene forebear, that modern mammals are clearly competitively superior to their Palaeo­ cene ancestors . This notion of progress is frequently assumed by biologists and palaeontologists, but is probably impossible to test directly . Nevertheless, simple assumptions of progress of this kind have

2 . 5 Red Queen Hypothesis been criticized recently (Benton 1987) . There seems to be no adequate way yet of demonstrating 'pro­ gress' in macroevolution, least of all competitive improvement. The evolution of horses can be taken as a well known example of an adaptive trend, or record of improvement through time . The early small leaf-eating horses of Eocene times gave way to larger animals with fewer toes (greater running speed) and deeper teeth (for grinding up the new silica-bearing grasses) in the Miocene (Section 1 . 1 1 ) . However, i f the fossil record were reversed, we could equally well demonstrate how the horses adapted to the diminishing grasslands by becoming smaller forest-dwellers, living a cryptic life and switching to a diet of tree leaves. Where is the progressive improvement of competitive ability? The whole question seems to hinge on how macro­ evolution is viewed . If organisms are generally very well adapted, finely tuned by natural selection, and if the physical environment has only minor effects, the Red Queen Hypothesis has to hold . If, on the other hand, organisms are viewed as only moder­ ately well adapted, natural selection as only a spor­ adic force for evolutionary change, and the physical environment as an important influence through local and global extinction, and radiation events, then the Red Queen Hypothesis cannot be correct. In 1984 Stenseth and Maynard Smith formalized an alternative to the Red Queen model, termed the Stationary Model. This model assumes that evo­ ution is driven mainly by abiotic factors, and that it will cease in the absence of changes in the physical environment . The two models make very different predictions and, as Stenseth and Maynard Smith (1984) wrote, 'the choice between the Red Queen and Stationary Models will have to depend primar­ ily on paleontological evidence' . The Red Queen model predicts that the rates of speciation, extinction, and phyletic evolution will remain constant in ecosystems, even when the diversity of species has reached equilibrium so that the numbers of species do not change . The Station­ ary Model, however, predicts that at equilibrium no evolution will occur . Bursts of evolution, extinction, and speciation will happen only in response to changes in the physical environment. These two models can be visualized by plots of species sur­ vivorship over time, which gives a measure of the rate of extinction (Fig . 2A, B) .

Testing the models Hoffman and Kitchell (1984) applied a palaeonto-

121

logical test. The first problem they encountered was to find an example spanning several million years in which no environmental change had occurred . Such a case i s highly unlikely, and it proved neces­ sary to make allowances for episodic perturbations in the physical environment. The modified patterns are still distinctive (Fig . 2C, D) . The Red Queen model predicts an approximately regular decline in the number of species surviving (that is, constant extinction), with occasional changes of slope that correspond to major environmental perturbations . The Stationary Model predicts a distinctly stepped pattern, with constant numbers of species at equilibrium, and sudden extinctions at times of environmental change . Hoffman and Kitchell (1984) also examined the records of microfossils (coccoliths, foraminiferans, radiolarians, diatoms, and others) from 1 1 1 deep­ sea boreholes through the past 50 million years of sediments of the Pacific Ocean floor. The species survivorship curves obtained from these data (Fig . 3) are more or less smooth, rather than stepped, and they seem to support the Red Queen model . An analysis of the cumulative appearance of new species also gave general support to the Red Queen model, although there was some evidence of stepping . Further analysis shows there to be considerable variation in the probability of extinction over geo­ logical time : for example, there seem to have been particular periods in which all the microfossil groups had high extinction rates. These indicate plankton extinction events which would normally be attributed to sharp changes in the physical environment . When Hoffman & Kitchell (1984) made allowances for these events, the various analyses again pointed to the Red Queen model. Another test, also using the plankton record, was carried out by Wei & Kennett (1983) . Their study was based on the fossil record throughout the world of 149 species of foraminifera over the past 24 million years. They found that major changes in rates of extinction and speciation corresponded to palaeoceanographic perturbations (Fig . 4), and they regarded their data as consistent with the Stationary Model . These two studies illustrate some of the practical difficulties involved in testing the Red Queen model . One serious problem is in separating biotic from abiotic factors in order to assess their relative significance : it is probably impossible to pigeon­ hole both kinds of phenomena as independent factors . Secondly, in many real situations, and pos-

2 The Evolutionary Process and the Fossil Record

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sibly including the two described above, the test would be inconclusive . For example, it would be hard to distinguish between two predicted patterns if both curves were stepped as a result of rapid changes in the physical environment. At the other extreme, continuous small changes in environ­ mental conditions might give similar gently sloping graphs for both models . Furthermore, as Hoffman and Kitchell (1984) pointed out, both the Red Queen and Stationary models assume that ecosystems tend towards a diversity of species that is at equilibrium . Both hypotheses predict that the total number of species is constant: the addition of one species to the system causes the loss of another . Yet models that do not assume such an equilibrium could also account for the Law of Constant Extinction and for the other palaeontological data . In these models, there would

5 S p e c i e s d u rat i o n

10

Predictions o f the Red Queen and Stationary models for species survivorship in constant (A, B), and periodically disturbed (C, D) environments. (After Hoffman & Kitchell 1984 . )

be no necessary limit to diversity, and the rates at which species arise or go extinct would not be correlated with each other, nor with total diversity. The data so far are equivocal on these points . Other research seems to count against the Red Queen Hypothesis . Kitchell et al. (1989) studied a simple predator - prey relationship : naticid gastro­ pods and bivalves . The naticid gastropods prey on bivalves by boring through their shells and extract­ ing the flesh . Both groups are plentiful as fossils, and such predation has left identifiable borings in fossilized bivalve shells . Kitchell and her colleagues modelled the predator -prey system mathematically and found that, whatever the starting point, the system tended to a static position . The bivalves evolved either to reproduce early (before they were eaten) or to devote all of their energy to building a thick shell to minimize the chance of successful

123

2 . 5 Red Queen Hypothesis

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124

2 The Evolutionary Process and the Fossil Record

boring attacks . This result speaks against the Red Queen model, which would require constant evo­ lution in a particular direction . Other biologists have argued that species prob­ ably do not keep running towards unattainable goals, as the Red Queen Hypothesis predicts . Each species is faced with the need to make compromises . Many bivalves, for example, have to balance the need for a strong shell against the costs of a heavy shell . The compromise solution is to have a thin corrugated shell. 'Constant running' in one direc­ tion is often not possible in a lineage, and the simplistic view of the Red Queen model as con­ tinuous and endless evolution in one direction may be denied by the limitations of genetic variation, development, and mechanical design factors .

References Benton, M.J. 1987. Progress and competition in macroevo­ lution. Biological Reviews 62, 305- 338. Hoffman, A. & Kitchell, J.A. 1984 . Evolution in a pelagic planktic system: a paleobiologic test of models of multi­ species evolution. Paleobiology 10, 9 - 33 . Kitchell, J . A . , DeAngelis, D . L . & Post, W . D . 1989. Predator­ prey interactions on the ecological and evolutionary time scale . In: N . C . Stenseth (ed . ) Coevolution in ecosystems and the Red Queen Hypothesis. Cambridge University Press, Cambridge. Stenseth, N . C . & Maynard Smith, J. 1984. Coevolution in ecosystems: Red Queen evolution or stasis? Evolution 38, 870 - 880. Van Valen, L . M . 1973. A new evolutionary law . Evolutionary Theory I, 1 -30. Wei, K-Y . & Kennett, J.P. 1983 . Nonconstant extinction rates of Neogene planktonic foraminifera . Nature 305, 218-220.

2 . 6 Hierarchy and Macroevolution N . ELDREDGE

Introduction Evolution is the scientific explanation of the design apparent in organismic nature . Natural selection is generally seen to be the principal cause of determin­ istic modification of the phenotypic properties of organisms through time . Macroevolution most commonly connotes the degree of such modification, and thus in its most general sense is simply 'large­ scale genotypiclphenotypic change' . Microevo­ lution, in contrast, refers to the relatively slight amount of change that occurs on a generation­ by-generation basis through natural selection and genetic drift . A connotation of elapsed time is often implicit in the distinction between micro- and macroevolution: microevolution takes place in relatively short amounts of time (e . g . 'ecological time,' over a few generations), while macroevolution is generally held to occur in geological time . Yet some theories of macroevolution (e . g . saltation theories of the geneticist R. Goldschmidt, or the palaeontologist O . Schindewolf) invoke brief (even single generation) genotypic and phenotypic trans­ formation . A further distinction commonly drawn

between 'microevolution' and 'macroevolution' sees the former as a within-species or perhaps within­ genus level phenomenon, in contrast with the degree of change associated more typically with the emergence of taxa of higher categorical rank (i . e . in the Linnaean hierarchy - families, orders, classes, etc . ) . The 'evolutionary synthesis', dating from the mid nineteen-thirties, forms the core of modern evo­ lutionary theory . The synthesis followed the succes­ sful fusion of Darwinian selection with an emer­ ging understanding of the principles of heredity (achieved primarily through the efforts of geneticists R.A. Fisher, J . B . S . Haldane and S. Wright) . This neo-Darwinian paradigm of drift- and selection­ mediated dynamics of genetic stasis and change was then integrated with the data of systematics, palaeontology, and other biological subdisciplines to form what was widely heralded as a unified theory of evolution . It is the general position of the synthesis that 'macroevolution' is simply microevo­ lution summed over geological time . Specifically, generation-by-generation stability and transform­ ation, mediated by natural selection and genetic

2 . 6 Hierarchy and Macroevolution drift, were held to be both necessary and sufficient to account for all aspects of the evolutionary history of life . Though the geneticist Dobzhansky (1937) and the systematist Mayr (1942) both sketched versions of macroevolutionary theory, it was left primarily to the palaeontologist Simpson (1944, 1953) to formu­ late the principles of macroevolution within the synthetic theory. The assumption that microevolution yields a complete account of the evolutionary process when projected over evolutionary (geological) time restricts the study of evolutionary mechanics to laboratory and field investigations of living organ­ isms . The role of palaeobiology in such a scheme, however, is by no means thereby rendered trivial: as Simpson (1944), for example, endeavoured to show, the integration of evolutionary theory with patterns of evolutionary events drawn from the fossil record is no simple matter. In particular, Simpson was concerned to show that it is the task of palaeontology to determine the relative intensities, and importance, of various microevolutionary pro­ cesses (e .g. mutation rate, selection, population size, etc . ) required to explain various evolutionary patterns of the fossil record . In that spirit, Simpson developed his model of 'quantum evolution' (rapid, 'all-or-nothing' modification of adaptive features of organisms in relatively small populations) to explain the relatively abrupt appearance so typical of many higher taxa . Recent years have seen an alternative view emerge on the relationship between palaeontologi­ cal data, geological time, and theories of the evo­ lutionary process. In traditional evolutionary biology, it is the phenotypic (and underlying gen­ etic) properties of organisms that are of central interest, and which 'evolve' . Organisms vary in these respects within local populations; populations are aggregated into species (Section 2.2). Natural selection 'sorts' the phenotypic attributes of organ­ isms within populations to yield (1) stasis or change in phenotypes, and (2) the emergence of new species (and, by simple extension, higher taxa) . 'Hierarchy theory' accepts the neo-Darwinian paradigm of within-population variation, selection, and drift, but seeks to extend the list of evolutionary entities beyond genes, organisms, and populations . Specifically, species, monophyletic (higher) taxa, and ecosystems have come to be viewed as having real existence, and are variously termed 'systems', 'entities', or even 'individuals' . The goal of hierarchy analysis is to elucidate the nature of each kind of large-scale entity, and thus to determine their pos-

125

sible role(s) in the evolutionary process. If large-scale systems such as species, higher taxa, and ecosystems are real entities, they exist on a spatiotemporal scale which is too large to be encom­ passed in laboratory and field experimental studies of the Recent biota. It is the fossil record that reveals the actual dimensions of such systems, and thus it falls in large measure to palaeobiology to examine how they can be integrated with existing theories of the evolutionary process. Such work has two aspects : (1) the determination of any relevance of such large-scale systems to the original problem of evolution - that is, the origin, maintenance, and further transformation of adaptive phenotypic fea­ tures of organisms; and (2) the recognition of other effects on the general history of life that may result from the existence of such larger-scale entities . Specifically, the concept that large-scale systems such as species, taxa, and ecosystems are them­ selves entities, not merely epiphenomena or simple (and perhaps arbitrarily delineated) collectivities of organisms, has led to several palaeobiological theor­ ies that allege a degree of additional process to macroevolution, over and above - and in some instances 'decoupled' from - microevolutionary processes.

Hierarchies in evolutionary biology Several meanings of the term 'hierarchy' are in general use in biology (Grene 1 987) . In the context of evolutionary theory, however, only two hierarchi­ cal systems are generally recognized: the genealogi­ cal and ecological (economic) hierarchies (Table 1 ) . Both are thought to b e implicated in the evolution­ ary process (Eldredge 1985, 1986, 1989; Salthe 1985), though some authors recognize one hierarchy and not the other. Both hierarchies consist of nested sets of entities forming distinct levels . Each level consti­ tutes a class (or category - e . g . 'species'), specific examples of which are entities or 'individuals' (e . g . Archaeopteryx lithographica) . The entities o f any given level have as parts the entities of the adjacent lower level and form, in turn, parts of the adjacent higher level: demes have organisms as parts; in turn, demes are parts of species . The entities a t each level interact o r behave in specific ways that unite them to form the entities of the next higher level . In the genealogical hierarchy the activity is 'reproduction' in the most general sense; thus, speciation is seen as the production of more entities (i . e . species) of like kind - an activity ultimately responsible for the ongoing existence of

126 Table 1.

2 The Evolutionary Process and the Fossil Record The genealogical and ecological hierarchies .

Genealogical hierarchy

Ecological hierarchy

Monophyletic taxa Species Demes Organisms Germ linea

Biosphere Ecosystems Avatars (populations) Organisms Somab

Composed of hierarchically nested chromosomes, genes, codons and base pairs. b Composed of hierarchically nested organ systems, organs, tissues, cells and proteins. a

higher taxa . In the economic hierarchy, direct inter­ action among entities of any given level cohere the entities of the adjacent higher level; thus it is the interaction among local populations of non­ conspecifics (as in predator -prey interactions) that unites them into local ecosystems . The two hierarchies arise out of the two types of organismic activity, that is reproduction, on the one hand, and processes related to matter - energy trans­ fer on the other. Viewed in this light, Darwin's distinction between sexual and natural selection is clear. In sexual selection, relative reproductive success arises strictly from among-population vari­ ation in some aspect of reproductive behaviour, physiology, or anatomy . In natural selection, an organism's relative success in economic (matter ­ energy transfer) activities has an effect on that organisms's probability of successful reproduction . The two hierarchies are direct outgrowths of these two distinct categories of adaptation that arise under sexual and natural selection. In sexual organisms, reproduction implies a local pool of suitable partners - a 'deme' . In most instances, there will be pools of suitable partners elsewhere; thus local demes form regional 'species' . Most modern treat­ ments of species recognize them as reproductive communities, within which mating occurs, outside which it does not. Paterson (e . g . 1985) recently suggested that species are reproductive com­ munities composed of organisms sharing a particu­ lar set of reproductive adaptations, or 'specific mate recognition system' ('SMRS') . His concept obviates the ambiguity of disjunct distributions, where potential mates never meet. Moreover, because the SMRS is an adaptive system subject to (sexual) selection (favouring mate recognition in isolation) speciation minimally must entail (presumably allo­ patric) divergence of the SMRS . Speciation is seen

as an outgrowth simply of continued reproduction in isolation, leading to modification of the SMRS . Because new (sexual) species arise in this fashion as a matter of course, higher taxa are maintained (as long as speciation rate exceeds extinction rate) . Higher taxa are seen strictly as lineages of species; they are recognized (just as are clones of strictly asexual organisms) only when new adaptations ('synapomorphies' of phylogenetic systematics; Section 5 . 2 . 2) arise and serve as markers for the lineage . As such, monophyletic taxa do not 'repro­ duce', that is, they do not produce additional entities of like kind . Genera do not give rise to new genera, the way that new species arise from old . The economic activities of organisms of a species lead them to form local populations ('avatars') which may, but need not, be coextensive with local demes of the same species . But above this level (Table I), a crucial distinction between the genealogical and economic hierarchies arises . Whereas the repro­ ductive adaptations of organisms are shared by organisms in other demes elsewhere, the economic adaptations of organisms lead to cross-genealogical interactions between local populations belonging to different species . Local ecosystems interact with other such systems on a regional scale, but maps of genealogical systems and economic systems simply do not coincide . It is especially significant that species are not parts of economic systems . Thus, by sheer dint of the existence of two classes of organ­ ismic activity - hence adaptations - organisms are simultaneously parts of two separate, hierarchi­ cally arranged systems . And in particular, inter­ action within and between entities of the two different hierarchies is of the greatest importance in elucidating a full causal theory of the evolutionary process .

The evolutionary process: role of the genealogical and economic hierarchies Discussions of macroevolution traditionally empha­ size the origin of higher taxa in the context of large­ scale adaptive change . Under this synthesis, linear trends are often said to be generated by 'orthoselec­ tion', i . e . long-term, predominantly directional natural selection, as distinct from 'orthogenesis', or linear phyletic change through unspecified causes internal to organisms . In general, the accumulation of significant amounts of adaptive transformation within a lineage has been termed anagenesis, which is commonly, if not invariably, held to be a process distinct from cladogenesis, or lineage splitting . Thus

2 . 6 Hierarchy and Macroevolution much, if not all, macroevolutionary change has tra­ ditionally been considered to occur without any (or any significant) degree of speciation . A major excep­ tion to this generalization is the theme of adaptive radiations, in which morphological transformation proceeds rapidly and independently in several or many different directions, and lineage-splitting is directly invoked as part of the process . Simpson's (1944) earliest formulation of 'quantum evolution' also invoked lineage splitting (though not expressly termed 'speciation'); later (Simpson 1953) modified in favour of a purely phyletic conceptualization of quantum evolution . The hypothesis of punctuated equilibria (Eldredge & Gould 1972) is based, in part, on the empirical claim that most species exhibit relative morphologi­ cal stability throughout the bulk of their strati­ graphic ranges (see also Section 2 . 3) . Thus most anatomical change appears to occur along with speciation . Such species stability facilitates recog­ nition of species as spatiotemporally-bounded enti­ ties; it further leads to the postulate that linear trends in macroevolution may reflect processes of species sorting in addition to directional natural selection . In general terms, such a model proposes that actual transformation of morphology occurs via directional natural selection (plus, perhaps, genetic drift) on a standard generation-by-generation basis . But the linearity of the trend through long periods of time - when the species remain morphologically stable and vary among themselves with respect to the evolving trait - arises through sorting of vari­ ation among species through a variety of potential causes . The term 'species selection' itself embraces a number of variant conceptualizations . As devel­ oped as an outgrowth of punctuated equilibria (Eldredge & Gould 1972); the term itself was intro­ duced by Stanley 1975; see also Stanley 1979), 'species selection' was virtually synonymous with the more general term 'species sorting' used here . Subsequent authors, seeking more precise parallel usage between organismic and higher-level selec­ tion, contend that 'species selection' is applicable only to species-level properties of species (cf. Vrba 1984) . This argument holds that phenotypic (and underlying genotypic) properties of organisms are the focus of organismic selection. True species selection should be invoked only to explain species­ level adaptations; it cannot logically be applied to the situation in which species differ merely in the frequencies of one or more organismic phenotypic traits . Williams (1966) was the first to argue this

127

point, claiming that 'group selection' can pertain only to group-level adaptations . Jablonski (1987) argued that geographical ranges are species-level properties, and show high heritability in his data on Cretaceous molluscs; he concluded that species ranges are therefore subject to true 'species selection' . Hull (1980) has discussed two components that must be present for selection to occur at any level; these two components serve in addition as criteria for evaluating claims of species-level selection . According to Hull (1980), among entities involved in any instance of selection, there must be an inter­ actor as well as a replicator. The relative success of interactors is recorded in the subsequent represen­ tation of their underlying replicators . Thus, in natural selection, relative economic success of organisms will affect their relative reproductive success, and hence the frequencies of the underlying genotypes . Organisms in this instance are both interactors and 'reproducers', with replicative fid­ elity supplied by their genes . Hull's (1980) selection criteria imply that species selection cannot be directly analogous to natural selection . If species are genealogical entities (if, in other words, it is the reproductive activities of organisms that lead to the formation and continued existence of species), species are causally connected to the replicative activities of genes; but if it is further true that species, as whole entities, do not play direct roles in ecological systems, species cannot be said to be interactors, and Hull' s criteria for selection are not met by definition for species . 'Species selection' appears t o b e most analogous to Darwin's sexual selection - because factors affecting rates of speciation and species extinction are involved . Species sorting i s a function of differential extinc­ tion and origination of species within a mono­ phyletic clade . It is the goal of macroevolutionary theory to specify the causal processes underlying such sorting. In addition to processes at work within a given level, the entities above and below in the hierarchy provide constraints (initial, or boundary conditions) on processes occurring within any given level - the 'upward and downward causation' of many hierarchy theorists . Vrba's (1980) 'effect hypo­ thesis' is an example of upward causation within the genealogical hierarchy . The effect hypothesis postu­ lates that macroevolutionary patterns (for example, linear trends in one or more morphological attributes within a clade over geological time) may arise simply as an outgrowth (side effect) of the

128

2 The Evolutionary Process and the Fossil Record

biology of the organisms themselves. Nothing more - specifically, no selection at the species level - need be invoked as an explanation of such patterns . Palaeontologists have sought links between characteristic speciation and extinction rates in lineages (macroevolutionary patterns), on the one hand, and aspects of organismic biology on the other - at least since Williams (1910) noted the apparent correlation between variation, niche width, and stratigraphic duration. Williams claimed that broadly niched (eurytopic) species, in addition to their characteristically wider geographical (habitat) occurrence, tend to display greater morphological variability (both within and certainly among populations) and longer stratigraphic dur­ ations than more narrowly niched stenotopes . Focusing especially on aspects of niche-width, macroevolutionary theorists have attempted to account for rates of both speciation and extinction. It seems, for example, that lineages comprised pre­ dominantly of eurytopic species show lower rates of species extinction and origination than lineages comprised of predominantly stenotopic species (see Eldredge & Cracraft 1980) . The contrast is especially clear in sister-lineages . Indeed, Vrba (1980) used the Miocene - Recent sister lineages of Aepycerotini (impalas) and Alcelaphini (wildebeests, hartebeests, topis, etc.), the former species-poor and eurytopic, the latter speciose, with short-ranging stenotopic species, to illustrate one possible cause underlying the 'effect hypothesis' (see also Section 2 . 10) . Vrba postulated that the trends in alcelaphine evolution were simply aggregates of higher rates of speciation and the accumulation of adaptive modification in the lineage of stenotopes - while little signifi­ cant evolutionary transformation accumulated within the co-ordinate lineage of eurytopes, the aepycerotines .

Interhierarchic interaction and macro evolution Darwin's (1859) original formulation of natural selection (where relative economic success affects relative reproductive success within a local popu­ lation of a species) serves as a model of the mech­ anics of interaction between the two hierarchies in the evolutionary process. Organisms, as members simultaneously in both the economic and genealogi­ cal hierarchies, patently stand as the prime causal link between the two (although some hierarchy theorists (notably Salthe 1985) see direct causal

interaction between entities at various levels of the two hierarchical systems) . Under the synthesis, species and higher taxa are generally depicted as having niches (or 'adaptive zones' in the case of higher taxa); further, in a widely used extension of Wright's (1932) metaphor of 'adaptive peaks', species and higher taxa are generally depicted as occupying peaks, or series of adjacent peaks (i . e . in an 'adaptive range') . Thus the most general approach to macroevolution under the synthesis holds that species and higher taxa are distinctly economic entities - effectively collapsing the dual hierarchy system into a single scheme . Yet, following arguments outlined above, it has seemed to recent theorists that species and higher taxa are different sorts of entities from those that form complex biotic economic systems . Species are aggregates of local demes, all of which share a common fertilization system. From an ecological point of view, species are typically integrated into a variety of different ecosystems . Yet organisms with­ in a species, as a rule, retain sufficient similarity in terms of economic adaptations that local populations are, to a great degree, redundant from one another. That is to say, the actual ecological role played by species is to serve as a reservoir of genetic infor­ mation. Local populations are notoriously ephem­ eral; local extinction, on several geographical and temporal scales, is often counteracted by recruitment from neighbouring demes. An important conse­ quence of the mere existence of species is that local parts of ecosystems are continually replenished from demes elsewhere . Recent studies of larval recruit­ ment in intertidal communities - after events that range from slight to total disruption - amply bear out the role that species play as reservoirs of genetic information . Darwin (1871) called species 'permanent varieties' . The expression is apt in the context of macro­ evolution, because the complexion of ecosystems is forever modified upon the final extinction of a species; the possibility of replacing local populations with conspecifics is forever lost. In general, just as species display a within-species pattern of supply of organisms to replace local populations, following extinction events that result in the loss of many higher taxa, the identities of the surviving taxa determine the natures of the sub­ sequently founded ecosystems . Disruption of eco­ systems results in extinction - the more severe the disruption, the higher the characteristic level of disappearance of taxa, from species on up; and the higher the average level of taxonomic extinction,

2 . 6 Hierarchy and Macroevolu tion the greater the change in economic systems . Theories (e . g . the 'Red Queen Hypothesis', Sec­ tion 2.5) often depict evolution as a process of inexorable adaptive change . Recent empirical and theoretical work in palaeobiology suggests rather a different picture : the ecological systems of which all organisms are parts, are formed from whatever organisms are extant at any given moment . With normal, small-scale fluctuations in composition and relative abundance of organisms, ecological systems appear to be quite stable . Speciation and extinction do occur, and so affect the composition of eco­ systems . Some phyletic modification may accrue within species, but, because most demes are ephemeral, little net change typically accumulates within species throughout most of their histories . Little in the way o f concerted evolutionary change, either within species or among species within lineages, tends to occur unless and until external perturbation disrupts ecosystems to the point where entire species - and higher taxa - become extinct, rendering impossible the resumption of ecosystems of the same composition as before . Thus, although the presence of genealogical entities (species and higher taxa - as packages of genetic information) are indispensable to the formation and ongoing existence of ecosystems, it appears that it is pri­ marily the disruption of such economic systems that leads to significant amounts of change within entities of the genealogical hierarchy . Hence mass extinction appears to be an important causal cornerstone of macroevolution .

References Darwin, C . 1 859 . On the origin of species . J. Murray, London . Darwin, C . 1871 . The descent of man, and selection in relation to sex. J. Murray, London. Dobzhansky, T. 1 937. Genetics and the origin of species. Columbia University Press, New York. Eldredge, N. 1985 . Unfinished synthesis . Oxford University

129

Press, New York. Eldredge, N. 1986. Information, economics and evolution. Annual Review of Ecology and Systematics 17, 351 - 369 . Eldredge, N. 1989 . Macroevolutionary dynamics: species, niches and adaptive peaks . McGraw-Hill, New York. Eldredge, N. & Cracraft, J. 1980. Phylogenetic patterns and the evolutionary process . Columbia University Press, New York. Eldredge, N. & Gould, S.J. 1972. Punctuated equilibria: an alternative to phyletic gradualism. In : T.J.M. Schopf (ed . ) Models i n paleobiology, pp . 82 - 1 15. Freeman, Cooper & Co . , San Francisco. Grene, M. 1987. Hierarchies in biology. American Scientist 75, 504-510. Hull, D.L. 1980. Individuality and selection. Annual Review of Ecology and Systematics 11, 31 1 - 322. Jablonski, D . 1987. Heritability at the species level : analysis of geographic ranges of Cretaceous mollusks . Science 238, 360 -363 . Mayr, E. 1942 . Systematics and the origin of species . Columbia University Press, New York. Paterson, H . E . H . 1985 . The recognition concept of species. In: E . S . Vrba (ed. ) Species and speciation, pp . 21 - 29 . Transvaal Museum Monograph No. 4. Transvaal Museum, Pretoria. Salthe, S.N. 1985 . Evolving hierarchical systems. Columbia University Press, New York. Simpson, G . G . 1944. Tempo and mode in evolution . Columbia University Press, New York. Simpson, G . G . 1953 . The major features of evolution . Columbia University Press, New York. Stanley, S . M . 1975 . A theory of evolution above the species level. Proceedings of the National Academy of Science 72, 646-650 . Stanley, S . M . 1979 . Macroevolution: pattern and process. W.H. Freeman, San Francisco. Vrba, E . 5 . 1980. Evolution, species and fossils: how does life evolve? South African Journal of Science 76, 61 - 84. Vrba, E . 5 . 1984. What is species selection? Systematic Zoology 33, 318-328. Williams, G . c . 1966. Adaptation and natural selection . Princeton University Press, New Jersey. Williams, H . S . 1910. The migration and shifting of Devonian faunas. Popular Science Monthly 77, 70 - 77. Wright, S. 1932. The roles of mutation, inbreeding, cross­ breeding and selection in evolution. Proceedings of the VIth International Congress of Genetics 1, 356- 366.

2 . 7 Patterns of Diversification P . W . SIGNOR

Introduction

fluence the composition of the fossil record . Sea­ level, which largely controls epicontinental marine deposition and preservation of fossils therein, has varied throughout the geological past. Low sea stands are usually represented in the stratigraphic record as diastems, disconformities, or unconform­ ities, and lack any fossil record of shelf faunas . Other time-dependent biases include monographic effects (Raup 1972) and the distribution of systematists' labour (Sheehan 1977) . There are significant time-independent biases. For example, terrestrial environments (and the organisms that inhabit them) are not well rep­ resented in the stratigraphic record, in comparison to marine habitats (e . g . Padian & Clemens in Valentine 1985) . Among marine organisms, heavily skeletonized forms are preserved far more fre­ quently than lightly or non-skeletonized forms . Palaeobiologists often presume that the ratio of heavily skeletonized to non-skeletonized species has been approximately constant, at least since the early Phanerozoic, but no data or arguments to support that contention have been advanced . On the contrary, there is some evidence that skeletons have become more robust in time in response to newly evolving predators (Section 4 . 13) . The net result of these biases is quite severe, amply justifying the ancient laments about the incompleteness of the fossil record . Only approxi­ mately 10% of the skeletonized marine species of the geological past and far fewer of the soft-bodied species are known (Sepkoski et al. 198 1 ; Signor in Valentine 1985) . No doubt whole clades and com­ munities of the past remain to be discovered. More importantly, these biases continue to obscure all but the most fundamental patterns in the history of diversification. A brief aside on the semantics of diversity might prevent confusion . The term diversity has been used in two senses . Unfortunately, the two usages are rather different, and treating the term carelessly confounds an important concept . In the palae­ ontological literature, diversity is often used to mean richness, or the number of taxa present. Diversity also has a second meaning, incorporating both rich-

The past 3 . 5 billion years have witnessed substantial change in the numbers of protist, animal, and plant taxa on Earth . The magnitude of that net change is evident from comparison of the lush biological diversity present in so many modem habitats with Archaean sediments seemingly barren of fossils . But reconstructing the geological history of organic diversity has proved difficult. Biases in the preser­ vation, collection, and study of fossils have com­ bined to obscure patterns of change in diversity. Despite the difficulties, a variety of different patterns of diversification has now been documented at scales ranging from local communities to the entire biosphere . These patterns indicate that the net accumulation of taxa through time has been quite unsteady .

Biases in the fossil record The geological history of taxonomic and ecological diversification is obscured by a variety of time­ dependent and time-independent filters . Most of these are various sorts of sampling biases, which cause the observed fossil record to differ from the actual history of the biosphere (see also Section 3 . 1 2) . The most severe of the time-dependent biases is the loss of sedimentary rock volume and area with increasing age (Raup 1976b) . Both sedimentary rock area and rock volume correlate strongly with the numbers of animal species described from that stratigraphic interval (Raup 1972, 1976b) . Rock volume and area affect apparent species richness by influencing the likelihood that a given species is preserved, discovered, and described (Raup 1976b) . Similar biases have been documented in the fossil record of vascular plants on land (Knoll et al. 1979) . The quality of preservation of fossils within sedi­ mentary rock also tends to deteriorate with increas­ ing age, because of extended exposure to diagenesis (Raup 1972) . The kinds of sedimentary rock and, by implication, the environments preserved in the stratigraphic record have varied greatly through time. Variability in the representation of palaeo­ environments in the stratigraphic record must in-

130

2 . 7 Patterns of Diversification ness and evenness of distribution. In this second sense, a community composed of three equally common species would be regarded as more diverse than a community of three species where one species far outnumbered the remaining two . The ecological literature generally restricts usage of diversity to the latter meaning. Most papers on the history of diversity, however, have treated diversity as synonymous with number of taxa present, and that is the approach used here .

Taxonomic diversity Tabulations of classes, orders, or families, instead of species, are commonly employed to minimize sampling bias in palaeontological estimates of bio­ logical diversity . One need only find a single species to document the presence of a higher taxon, whereas every species must be discovered to provide com­ plete documentation of species richness. Therefore, researchers have employed classes, orders, or families as surrogates for species in estimates of biological diversity in situations where our ability to sample species is hindered . Higher taxa have also been employed as metrics of morphological or ecological diversification (e.g. Erwin et al. 1987) . The utility of higher taxa as first order metrics of species richness is dubious (see Sepkoski 1978 for a contrary view) . Tabulations of marine orders and families (Sepkoski 1978, 1979, 1982) and estimates of species richness (Sepkoski et al. 1981; Signor in Valentine 1985) are not congruent, indicating that numbers of higher taxa do not parallel changes in underlying species richness (Fig . lA, B) . Generic diversity is rather similar to estimated patterns of species richness, but patterns of the diversity of families, orders, or classes are increasingly dissimi­ lar . Similarly, Raup's (1979) analysis of the Permo­ Triassic mass extinction (Section 2 . 13 .4) indicates that 17% and 52% reductions in the number of marine orders and families, respectively, represent approximately a 96% reduction in the number of species . Likewise, patterns in the numbers of ter­ restrial vertebrate orders are rather dissimilar from patterns in the numbers of genera (see Padian & Clemens in Valentine 1985) . Higher taxa are buffered from fluctuations in numbers of species and con­ sequently are poor metrics of changes in species richness. Higher taxa are more or less artificial constructs that are not defined by species richness . Indeed, most higher taxa incorporate relatively few species (Sepkoski 1978) . Therefore, the lack of concordance

131

200

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B

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Fig. 1 Diversity of marine animals. A, numbers of marine orders through time . (Data from Sepkoski 1978 . ) B, numbers of marine families through time . (Data from Sepkoski 1979 . ) C, percentage change i n the number o f marine genera through time . (Data from Sepkoski et al. 1981 . ) D, estimated percentage variation in the number of skeletonized marine invertebrate species. (Data from Signor in Valentine 1985 . )

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2 The Evolutionary Process and the Fossil Record

between the number of species, families, orders, or classes through time is not surprising . In contrast, biological species can be defined and recognized through patterns of reproductive isolation : they are real biological units . As an entity, the species possesses biologically significant characteristics lacking in higher taxa . But change in the numbers of species through time is a more difficult problem to attack than change in higher taxa, because of the inherent deficiencies of the fossil record (Section 3. 1 2) . The numbers o f Phanerozoic marine orders and families have been tabulated by Sepkoski (1978, 1979, 1982) (Fig. lA, B) . The number of orders in­ creased rapidly until the Late Ordovician, and then remained approximately constant for the remainder of the Phanerozoic. The number of families also increased rapidly in the Cambrian and Ordovician, reaching a plateau of about 400 families for the remainder of the Palaeozoic . Following the Permo­ Triassic mass extinction (Section 2 . 13 .4), the number of families has increased more or less continuously to the present . A preliminary tabulation of the number of genera shows a pattern generally similar to the change in numbers of families through time (Sepkoski et al . 1 981) (Fig . 1C) . Compilations of the number of described marine species through time show low numbers through the Palaeozoic and Mesozoic, followed by a sub­ stantial increase in the Cenozoic (Raup 1976a) . These tabulations are undoubtedly skewed by sampling biases, as discussed above (see Raup 1976b) . Attempts to infer patterns of species richness from changes in the numbers of higher taxa have produced patterns generally similar to Raup's tabulation, but show lower numbers of species in the Palaeozoic and Mesozoic. Analytical calculations to remove the effects of sampling bias result in a similar pattern (Signor in Valentine 1985; Fig . ID) . The history of diversification of terrestrial vertebrates produces a quite different pattern . Compilations of the numbers of tetrapod orders through time show no longstanding equilibrium (Padian & Clemens in Valentine 1985; Fig . 2A) . There was a steady increase through the Middle Palaeozoic, reaching a Mesozoic plateau that began in the Late Triassic . Following the Cretaceous ­ Tertiary mass extinction (Section 2 . 1 3 .6), the number of orders increased briefly and then began to decline (Fig. 2A) . The Tertiary adaptive radiation of birds is superimposed upon this diversification, and nearly doubled the number of terrestrial vertebrate orders (Fig . 2A) . The pattern at the generic level is similar,

but more exaggerated (Padian & Clemens in Valentine 1985) . The number of genera rose quickly through the Palaeozoic to a peak in the Permian . Following a severe reduction in generic diversity at the end of the Permian, the number increased, regaining Permian levels in the Cretaceous . In the Cenozoic the number of genera increased nearly tenfold . The history of the diversification of vascular plants forms still a third pattern (Fig . 2B) . In the Northern Hemisphere, there was a gradual increase in species richness to a peak of over 40 species early in the Late Devonian (Niklas et al. in Valentine 1985) . Following a slight decline in the Late Devonian, the number increased rapidly to over 200 species by the Middle Carboniferous . With the exception of a brief decline at the end of the Permian, the number of species increased gradually through the remainder 50 Terrestrial ve rteb rate o rd e rs

30

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Fig. 2 Diversity of terrestrial organisms. A, numbers of terrestrial vertebrates through time . Solid lines indicate changes in the number of amphibian, reptile, and mammal orders; dotted lines indicate the number of avian orders. (Data from Padian & Clemens in Valentine 1985 . ) The Cenozoic is subdivided into the five epochs of the Tertiary plus the Pleistocene . B, numbers of terrestrial plant species (mostly in the Northern Hemisphere) through time . (Data from Niklas et al. in Valentine 1985 . )

2 . 7 Patterns of Diversification of the Palaeozoic, the Triassic, Jurassic and Early Cretaceous. Following the origin of angiosperms (Section 1 . 10) in the Late Cretaceous, species rich­ ness increased rapidly to over 600 in the Quaternary . Patterns of global taxonomic richness differ at various levels of the taxonomic hierarchy. Unbiased species data would most accurately reflect changes in biological complexity through time, but species­ level data are the most susceptible to sampling bias. The species richness of marine animals, vascular plants, and terrestrial vertebrates have quite dif­ ferent histories, but all indicate significant re­ ductions in diversity at the Permo-Triassic, Norian, and Maastrichtian extinction events (Section 2 . 1 3) . All three patterns also share a tremendous diversification of species beginning in the Cretaceous .

Local diversity An important component of the history of diversity is the temporal pattern of species richness within individual communities . Bambach (1977) compiled counts of species present within 386 previously described ancient marine communities . He assigned the communities to one of three generalized habi­ tats : nearshore high stress, nearshore variable, and open marine environments . Alpha diversity, or within-community diversity, remained constant in the high-stress environment communities throughout the Phanerozoic, but increased twofold in the variable nearshore and open marine environ­ ments during the Mesozoic (Bambach 1977; Fig . 3C) . The Mesozoic increase in alpha diversity appar­ ently was accommodated through trophic diversifi­ cation of the major clades of marine animals in shelf communities (Bambach 1983) . In the Cambrian, there were relatively few clades and each clade had a limited range of roles . The number of clades increased in the Palaeozoic, an increase that was paralleled by a limited diversification of trophic roles . The Mesozoic increase in diversity was accompanied by a much larger diffusion of taxa into new trophic roles, especially into infaunal life­ modes . The expansion of marine animals into infaunal life-modes is one component of the pattern of increasing tiering (Section 1 . 7 . 1 ) . Tiering, the spatial development of communities both above and below the sediment surface, had increased through the Phanerozoic. This increase has been attributed to a number of physical and biological processes, but

133

the net result is undoubtedly an increase in local habitat complexity and organic diversity .

Controls on diversity The nature of the processes controlling species rich­ ness is the subject of considerable speculation. At the level of communities, such processes are not well understood, even in the modem world . Area, habitat complexity, environmental stability, physi­ cal disturbance, and other factors may well be important controls on alpha diversity . What tran­ spired to bring about a twofold increase in within­ habitat species richness in the late Mesozoic is equally unclear . A better understanding of the processes regulating species richness in the Recent is probably a prerequisite to resolving this question . Area is a primary influence on diversity at local, regional, and global levels . Area appears to regulate diversity primarily through variation in rates of extinction . Reduction in habitable area decreases population size, which increases the chance of extinction . For organisms dwelling among the benthos on continental shelves, change in diversity appears to be related to variation in shelf area (Sepkoski 1976; but see Flessa & Sepkoski 1978) . Severe reductions in shelf area have also been im­ plicated as the cause of a mass extinction (Sections 2 . 1 2 . 1 , 2 . 1 3 . 4) . Mass extinctions severely reduce the number of taxa present in the biosphere . Diversity generally rebounds following extinction events and often increases to surpass previous levels, but that re­ bound requires geologically significant intervals of time . The time necessary for recovery is, in part, proportional to the magnitude of the extinction (Sepkoski 1 984) . During the intervening time be­ tween extinction and recovery, diversity is reduced . I f extinctions are spaced more closely than the necessary recovery time, the biosphere will remain relatively impoverished (e . g . Hansen 1988) . At the level of the biosphere, plate tectonics is undoubtedly the most potent control on the diver­ sity of organisms (Valentine et al. 1 978; Signor in Valentine 1985) . Marine organisms often share com­ mon range boundaries, and geographical regions with relatively homogeneous faunas and distinct boundaries are termed provinces (see also Section 5.5) . The boundaries of these provinces are defined by the joint limits of distribution of common species, and are controlled by patterns of climate and oceanic water circulation. In turn, climate and oceanic circulation are determined largely by the

134

2 The Evolutionary Process and the Fossil Record

distribution of continental land masses. Continu­ ously changing continental configurations have thus regulated the number and distribution of provinces through time . Changing levels of provinciality have no apparent impact on biological complexity within individual communities, but alter global diversity through adding or subtracting whole provinces . The number of provinces has increased greatly since the late Mesozoic breakup of Gondwana and Laurasia (Valentine et al. 1978), a change undoubt­ edly responsible for much of the increase in species richness of marine animals . The species richness o f vascular plants and terres­ trial vertebrates is also heavily influenced by plate tectonics (e . g . Padian & Clemens in Valentine 1985) . Tertiary isolation of the terrestrial faunas of South America, Australia, Africa, and Madagascar permit­ ted the evolution and persistence of unique faunas, while other clades dominated the Hcilarctic continents of Asia, Europe, and North America . Isolation and interspersed periods of faunal inter­ change have contributed greatly to the diversity and taxonomic composition of the terrestrial vertebrate faunas of the different continents . In summary, local and regional patterns in the number of taxa vary semi-independently and are compounded at regional and global scales . Increas­ ing alpha diversity within marine communities resulted in a comparable increase in global diversity in the Late Mesozoic . Similarly, changes in provin­ ciality through time have altered global diversity . Changes at each level of the ecological hierarchy, from the community to the biosphere, influence trends in global diversity . Such trends therefore represent complex interactions of physical and biological processes operating on many scales.

Diversity within clades A systematic pattern of temporal change in diversity within individual clades has recently been recog­ nized (Gilinsky & Bambach 1987) . Clades appear to contain more subtaxa early in their histories than later on . The primary cause of this trend appears to be a systematic decline in rates of origination within established clades through geological time, although rates of extinction also increase somewhat through time (Gilinsky & Bambach 1987) . The obvious inference from this statistical generalization is that clades are established during brief adaptive

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radiations and subsequently begin a long decline to eventual extinction . Speciation, not extinction, might be the dominant factor in clade diversity (Gilinsky & Bambach 1987) .

2 . 7 Patterns of Diversification Modelling change in diversity through time Sepkoski (1978, 1979, 1984) applied quantitative models of population growth to the history of taxo­ nomic diversity of marine organisms . These models were developed to describe and predict the insrease in numbers of individuals within single popu­ lations . The mathematical assumptions of the simplest model, the logistic model of population growth, are : (1) there is a maximum number of individuals that can be supported in the environ­ ment (the carrying capacity); and (2) population growth is exponential and declines linearly as the population size approaches the carrying capacity . These assumptions may also reasonably apply to taxonomic diversification at the level of the bio­ sphere . Sepkoski's (1978) successful application of the logistic model to describe the increase in numbers of marine orders suggests that the model describes the behaviour of change in the numbers of orders rather well . Similar results have been obtained in analyses of the radiation of angiosperms (Lidgard & Crane 1988) . Further applications of more complex models from population biology treat different aggregates of clades as faunas, comparable to populations competing for resources (Sepkoski 1979, 1984) . These models also produce good fits with the available data .

Faunal equilibrium? Over the past 20 years, a number of theorists have questioned the empirical pattern of increasing species richness through time, suggesting instead that the diversity of marine animals has been at equilibrium through much of the Phanerozoic (see Signor in Valentine 1 985 for review) . In this view, changes in species richness reflect only biases and not biologically significant trends . The equilibrium itself could be absolute, with constant numbers of species through time, or dynamic, with an equilibrium shifting in response to the changing physical world. However, the similar patterns observed in a variety of separate metrics of diversity (Fig. 3) provide convincing evidence that the ap­ parent pattern of species richness through time is not artifactual (Sepkoski et al. 1981 ) . But important questions about historical patterns of local and global species richness, and the ultimate controls on those patterns, remain to be resolved.

135

References Bambach, R.K. 1977. Species richness in marine benthic environments through the Phanerozoic. Paleobiology 3, 152- 167. Bambach, R.K. 1983. Ecospace utilization and guilds in marine communities through the Phanerozoic. In : M.J.5. Tevesz & P . L . McCall (eds) Biotic interactions in Recent and fossil benthic communities, pp. 719 - 746. Plenum Press, New York. Erwin, D . H . , Valentine, J.W. & Sepkoski, J . J . , Jr. 1987. A comparative study of diversification events : the early Paleozoic versus the Mesozoic. Evolution 41, 1 1 77 - 1 186. Flessa, K.W. & Sepkoski, J.J., Jr. 1978. On the relationship between Phanerozoic diversity and changes in habitable area. Paleobiology 4, 359- 366. Gilinsky, N.L. & Bambach, R.K. 1987. Asymmetrical patterns of origination and extinction. Paleobiology 13, 427-445 . Hansen, T .A. 1988. Early Tertiary radiation of marine molluscs and the long-term effects of the Cretaceous ­ Tertiary extinction. Paleobiology 14, 37-51 . Knoll, A . H . , Niklas, K.J. & Tiffney, B . H . 1979 . Phanerozoic land-plant diversity in North America. Science 206, 1400- 1402 . Lidgard, S. & Crane, P.R. 1988 . Quantitative analyses of the early angiosperm radiation. Nature 331, 344-346. Raup, D . M . 1972. Taxonomic diversity during the Phanerozoic. Science 177, 1065 - 1071 . Raup, D . M . 1976a . Species richness in the Phanerozoic: a tabulation. Paleobiology 2, 279 - 288. Raup, D.M. 1976b . Species richness in the Phanerozoic: an interpretation . Paleobiology 2, 289 -297. Raup, D . M . 1979 . Size of the Permo-Triassic bottleneck and its evolutionary implications. Science 206, 217-218. Sepkoski, J.J., Jr. 1976 . Species diversity in the Phanerozoic: species- area effects . Paleobiology 2, 298 -303. Sepkoski, J . J . , Jr. 1978. A kinetic model of Phanerozoic taxo­ nomic diversity, I. Analysis of marine orders. Paleobiology 4, 223 -251 . Sepkoski, J . J . , Jr. 1979 . A kinetic model of Phanerozoic taxo­ nomic diversity, 11 . Early Phanerozoic families and multi­ ple equilibria. Paleobiology 5, 222 - 251 . Sepkoski, J . J . , Jr. 1982. A compendium of fossil marine famil­ ies. Milwaukee Public Museum Contributions to Biology and Geology No . 51 . Milwaukee Public Museum, Milwaukee . Sepkoski, J.J., Jr. 1984. A kinetic model of Phanerozic taxo­ nomic diversity, Ill. Post-Paleozoic families and mass extinctions . Paleobiology 10, 246- 267. Sepkoski, J . J . , Jr. , Bambach, R.K., Raup, D . M . & Valentine, J.W. 1981 . Phanerozoic marine diversity and the fossil record . Nature 293, 435 -437. Sheehan, P.M. 1977. Species diversity in the Phanerozoic: a reflection of labor by systematists? Paleobiology 3, 325 - 328 . Valentine, J.W. 1985 . Phanerozoic diversity patterns . Princeton University Press, Princeton. Valentine, J . W . , Foin, T . e . & Peart, D. 1978 . A provincial model of Phanerozoic diversity. Paleobiology 4, 55 - 66 .

2 . 8 Coevolution S . C O NWAY M O RRIS

Introduction

survivorship curves by L.M. Van Valen indicated that the rate of extinction is stochastically constant, i . e . the probability of extinction is constant irres­ pective of the duration of a particular taxon . Van Valen explained this pattern by the now well known Red Queen Hypothesis (Section 2 . 5), arguing that the environment in which evolution occurs is largely defined by biotic interactions that operate so that the improvement in fitness of any one species auto­ matically reduces the fitness of all others (given that the sum of all fitnesses remains unchanged) . In this sense ecological units consisting of numerous inter­ acting species, which exhibit unceasing evolution­ ary change as species attempt to restore their fitness in the face of a constantly deteriorating biotic en­ vironment, may be said to show coevolution . Whether the Law of Constant Extinction is empiri­ cally demonstrable, and whether the Red Queen Hypothesis is the appropriate explanation, have both been extensively debated . Recent analyses of planktic species (mostly coccoliths, foraminifera, and radiolarians) from Cenozoic ocean deposits from mid-to-Iow latitudes give some support to the Red Queen Hypothesis, although the data on species survival have to be considered in the context of an environment that is not effectively constant . There are three other areas in the fossil record that may be explained in the broad context of co­ evolution . These are claims for reciprocal patterns between: (1) predators and prey; (2) plants and animals, especially insects; and (3) phylogenetic congruence between symbiotic taxa, especially parasites and their hosts .

Ever since the first species was joined by a second one, the potential for some sort of coevolution has existed. However, the possibility of documenting coevolution in the fossil record depends on the scope of the definition that is accepted . In a broad sense, coevolution has been taken to include almost any biological interaction, with emphasis often placed on mutualistic associations . Stricter defi­ nitions emphasize reciprocal responses between individuals of two species where each exerts, either sequentially or synchronously, an influence on the other's heritable characters . Whether such coevolutionary oscillations are stable over geo­ logical periods of time is not certain, and it seems questionable whether coevolution in a strict sense has ever been recognized in the fossil record . Accordingly, evidence for more broadly based in­ teractions that seem in some sense to represent responses by one taxon or group to changes in another is presented here .

Gaia On the grandest scale there has been considerable interest in the concept of Gaia, whereby a system of organically mediated feedbacks maintains the Earth's surface in a state of homeostasis that is largely independent of external vicissitudes that otherwise would imperil the continuation of life . However, while it is accepted that biological activi­ ties can mediate geochemical, and probably geo­ physical, cycles, there has been less enthusiasm for the notion that life in toto could act as the primary regulator of Gaia . This is because individual species, rather than the entire biosphere, must be accepted as the units for evolutionary selection, with life exploiting those opportunities offered by changing environments .

Predators and prey Much interest has been expressed in the possibility of an arms race between predator and prey, with a spiralling escalation of attack and defence . There are, however, reasons to doubt that a long-term oscillation would persist . In particular, Vermeij (1982) pointed out that: (1) as most predators feed on at least several species, if confronted by an increasingly well-defended prey they will switch to one of greater vulnerability; and (2) the predator itself will be prey for other species, so that selective

The Law of Constant Extinction While not as grandiose in its scope, the so-called Law of Constant Extinction may have implications for interactions between members of entire ecologi­ cal groupings of taxa . Analyses of numerous taxon

136

2 . 8 Coevolution factors that favour the predator' s own survival, as against its ability to obtain a meal, will predomi­ nate . Indeed, the only cases where reciprocal evolution of prey and predator may show consistent trends are where a victim can on occasion maim or even kill its attacker. Notwithstanding the potential problems in documenting predator- prey arms races, a number of attempts have been made to demonstrate reci­ procity in the fossil record on the basis of broad­ scale trends. One of the best known analyses concerns changes in the brain mass of Cenozoic ungulate herbivore and carnivore mammals. From a study of brain sizes Jerison (1973) concluded that the carni­ vores maintained proportionally larger brains than the ungulates, although both showed a persistent increase during the Cenozoic. This pattern was explained by a type of coevolutionary feedback whereby selection pressure exerted by the larger­ brained carnivores forced a corresponding increase in the herbivores, which in turn fuelled further increases in the carnivores . The validity of this analysis, however, has been questioned . Radinsky (1978) pointed out that: (1) many of the comparisons involve carnivores and ungulates of different stratigraphic age; (2) the estimates of body weight (needed as part of the calculation of the relative brain size) may require revision; and (3) some samples may be too small to provide reliable comparison . He concluded that, where the data are adequate, supposed differences between ungulates and carnivore brain sizes can­ not be demonstrated . Moreover, other studies of mammalian evolution in the Cenozoic (Bakker in Futuyma & Slatkin 1983) have argued that while both carnivores and herbivores show trends towards greater efficiency (e . g . for running) the so-called adaptive gaps may widen, especially when replace­ ment faunas arrive following a mass extinction. Changes in predator- prey interactions have also been identified in the marine record (see also Section 4 . 1 3 . 1 ) . The rise of predators in the Cambrian is followed by an episode of increasing predatory activity in the Middle Palaeozoic and finally a major reorganization of prey and predatory ecologies during the Jurassic and Cretaceous (the so-called Mesozoic Marine Revolution) . However, apart from the parallel rise of offensive and defensive adap­ tations, it has not been possible to demonstrate specific series of reciprocal changes, and it seems that evolutionary responses may have been diffuse . Amongst invertebrates, recent research has investigated possible coevolution between preda-

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tory gastropods, especially naticids, and their prey of bivalve molluscs, which they attack by drilling through the shell (Kitchell in Nitecki & Kitchell 1986) . While evidence for naticid attacks may extend back to the Triassic, it first became widespread in the Cretaceous . Study of drilling behaviour demon­ strates a remarkable stereotypy over geological time in terms of both position on the prey and ability to resume attack after interruption . However, in terms of possible coevolutionary responses between predator and prey, the only persistent trend that can be documented in the fossil record is a mutual increase in size.

Plants and animals The widespread inference of coevolution between plants and arthropods, especially insects, in modem biotas has often been extended into the geological past. However, despite some classic examples, such as between figs and fig-wasps, there is serious reason to doubt whether many Recent plant­ animal interactions can be regarded as strictly coevolutionary. Nevertheless, there is a widespread assumption that the diversification of plants and insects in the fossil record has been governed by coevolutionary forces . At present only the growing evidence for plant- animal interactions can be documented, leaving open the question of whether any of the examples fall into the domain of strict coevolution . Evidence for such interaction can be traced to the early Devonian, both in the form of direct associ­ ations (e . g . trigonotarbid arachnids lurking in sporangia of Rhynia from the Rhynie Chert), and more generally in plant morphology that ostensibly either promoted (e . g . spore sculpture) or hindered (e . g . stem spines) arthropod interactions . In these latter cases caution must be exercised, as specific features of plant anatomy may have had multiple functions including resistance to water loss, shielding from ultraviolet radiation, and so forth . By the Carboniferous there is considerable evidence for plant- animal interactions, both direct, such as spores in insect guts or various trace fossils (coprolites, borings, chew marks), and indirect, from insect mouth parts or plant anatomy, especially of spores and seeds . However, in no case has it been demonstrated that either partner was exerting reciprocal selective pressure over a period of geo­ logical time . Evidence of responses to arthropods in younger floras (Crepet 1979) includes study of reproductive structures, such as those of cycads,

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whose cone anatomy appears to trend towards excluding insect attack. Particular attention has been given to the activities of insects in pollination, to which has been linked the rise of the bisporangiate condition. In the Jurassic gymnosperms, for example, coleopterans (beetles) may have been of particular importance, but with the rise of the angiosperms in the Cretaceous (Section 1 . 10) the role of dipterans (flies) and hymenopterans (bees and wasps) is regarded as crucial . In particular, links between insect group and flower or inflor­ esence anatomy may allow inferences on potential pollinators . However, in many examples the assumptions are based on uniformitarian premises and it is also important to realize that strict coevolution has not been demonstrated . Indeed, in many cases it is likely that evolution was sequential, the insects following plant diversificati0t:t rather than acting as primary mediators . Although the greatest interest in plant- animal coevolution has concerned the role of arthropods, speculation has extended also to vertebrates . Stebbins (1981) argued for coevolution between Cenozoic mammalian grazers (e . g . horses) and the grasses (see also Section 1 . 1 1 ) . The development of hypsodont teeth to cope with the siliceous grasses (specifically the secretion of opalines in the plant epidermal cells), and of running ability in more open savanna, would seem to be linked intimately with the spread of grasslands . However, reciprocal connection between degree of hypsodonty and silica content or distribution, that could be taken as strict coevolution, has not been demonstrated .

Phylogenetic congruence The final area where the fossil record may contribute to the documentation of coevolution is in the identification of congruent phylogenies where mutualistic associations, especially between para­ sites and their hosts, are reflected in their respective histories of cladogenesis (Mitter & Brooks in Futuyma & Slatkin 1983) . This pattern is often refer­ red to as Fahrenholz's Rule, but to date the evidence for congruence has varied widely and in very few clades of parasite and host is strict congruence evident . Where parasites possess limited abilities for dispersal then host - parasite congruence may occur. However, if a parasite species is pursuing a particular feature, in what is known as resource tracking, then typically it will occur in those taxa that happen to share the particular resource . Thus, in the Mallophaga (chewing lice) the limited dis-

persal of those infesting some mammals (e . g . pocket gophers) contrasts to the distribution of those para­ sitizing birds, where feather type seems to be of particular importance (Timm in Nitecki 1983) . Where Fahrenholz' s Rule appears to be applicable, then in principle the fossil record of a well skeletized host could give insight into the evolutionary history of the parasites, which are almost invariably soft­ bodied and unknown as fossils . While the fossil record may throw light on times of divergence in such instances, the relatively few well documented lineages still only provide a broad indication of evolutionary events, and tightly constrained his­ tories do not appear to be available . The numerous commensal associations that have been documented may prove a more fruitful area for establishing phylogenetic congruence between symbionts in the fossil record . These include host specific epizoans, e . g . cornulitids, spirobids and other 'worms', and more intimate associations such as those between stromatoporoids and corals . However, in no case does it appear that strict coevolution has occurred, and in at least some cases there is evidence that the host has evolved (at least morphologically) at a substantially faster rate than its partner.

Conclusion While evidence of species interaction is manifest in the fossil record, examples of strict coevolution have yet to be documented . This may reflect problems of resolution and insufficient study, but it seems more likely that long term associations only rarely fall into the category of coevolution as it may be usefully understood .

References Crepet, W.L. 1979 . Insect pollination: a paleontological per­ spective. BioScience 29, 102 - 108. Futuyma, D.J. & Slatkin, M . 1983 . Co-evolution . Sinauer, Sunderland, Massachusetts. Jerison, H.J. 1973 . Evolution of the brain and intelligence. Academic Press, New York. Nitecki, M.H. (ed . ) 1983. Co-evolution . University of Chicago Press, Chicago. Nitecki, M . H. & Kitchell, J . A . (eds) 1986 . Evolution of animal behavior: paleontological and field approaches . Oxford University Press, New York. Radinsky, L. 1 978. Evolution of brain size in carnivores and ungulates. The American Naturalist 112, 815 - 831 . Stebbins, G . L . 1981 . Coevolution of grasses and herbivores . Annals of the Missouri Botanical Garden 68, 75 -86. Vermeij, G.J. 1 982. Unsuccessful predation and evolution. The American Naturalist 120, 701 - 720 .

2 . 9 Adaptation P . W . SKELTON

adequacy in the face of competition becomes the expected rule . Persistent competition may eventu­ ally perfect some adaptations, but there are many reasons, ranging from environmental change to the inherent constraints of bodyplans, why others are not perfected . B y limiting the notion o f function t o the effect of any given feature on the lives of its possessors, and by placing natural selection in the creative driving seat of evolution, Darwinism avoids the teleology, and thus the unacceptable mystery of earlier explanations of adaptation . Evolutionary thinking requires a distinction be­ tween adaptation as a process of gradual modifi­ cation in a population, and as a state of being in individuals, in relation to prevailing circumstances . With natural selection, the state o f being adapted, in respect of some feature or complex of features, also takes on two aspects: first, there is the element of function - the way in which the feature or complex operates - and, second, there is the selec­ tive benefit to the possessors of the feature or com­ plex, in terms of preferential survival and/or fecundity, deriving from its operation . Varying emphasis on one or other aspect in different usages of the term 'adaptation' has led to much confusion and misunderstanding; so it is worth teasing them apart somewhat. Darwin himself still used the term in an essentially vernacular fashion, primarily stres­ sing functional suitability: the 'best adapted' were simply those individuals possessing the most 'useful' variations for the operation of various life functions, such as feeding, locomotion, and seed dispersal. These, he repeatedly postulated, would tend to be favoured by natural selection in the 'struggle for existence', so fuelling the continuing process of further adaptation in populations . This Darwinian sense of adaptation, still recognizable independently of selective effects, though assumed to be both the product of, and producing them, is still widely used today, especially by palaeontol­ ogists, for reasons discussed below . Evolutionary biologists, on the other hand, have considerably refined the theory of natural selection and, in so doing, have subtly redefined the meaning of adaptation precisely in terms of selective effects .

Introduction Natural historians have long admired the ways in which the construction and activities of living organisms seem to be so well suited, or 'adapted', to the natural circumstances in which they live . Especially striking is the extent of co-operation of their features that renders them so adapted . Illustrations readily spring t o mind, such a s the stiffened tail, the two backward-pointing toes on each foot, the stout beak, and the extendible tongue of the woodpecker, which together enable it to perch on tree stems and probe them for insects . To most pre-Darwinian thinkers such adaptive traits were the essentially static attributes of fixed species, perfectly fitting them, perhaps by divine appointment, to their places in nature . Certain pre-Darwinian transformists, such as J-B . Lamarck and Erasmus Darwin, in contrast, postulated that the inheritance through many generations of habitually acquired developmental modifications (such as, say, the building up of well exercised muscle) was a means of evolutionary adaptation . But there has never been any satisfactory evidence for this . Both the static and the Lamarckian views of adaptation were teleological; that is to say they appealed to final causes in placing the prospect of a function (either in God's mind, or in the 'needs' or 'strivings' of organisms) prior to the appearance of the feature adapted for it. Such explanations, though still rife in the popular imagination, are categorically denounced by most biologists today because of the inherently untest­ able character of the final causes . The DarwinIWallace theory o f natural selection, on the other hand, asserted that adaptations be­ came established in evolving populations through the preferential survival and reproduction of indi­ viduals possessing naturally occurring, heritable variations, which conferred advantage in the 'strug­ gle for existence' arising from the excessive fec­ undity of the populations in relation to resources . This means that adaptation need not b e perfect, as earlier naturalists had tended to opine . Rather,

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Adaptation in evolutionary biology The 'neo-Darwinian synthesis' of the nineteen­ thirties to the nineteen-fifties attributed all evo­ lutionary adaptation to the operation of natural selection upon the phenotypic manifestations of genes in populations . Darwin's (and others') speculations on the additional operation of pro­ cesses other than selection (such as the effects of use and disuse, and other somatic influences on the germ line) were brushed aside . Statistical models of population genetics allowed the operation of natural selection to be quantified . 'Fitness', which to Darwin had been a somewhat vague expression of relative adaptedness of individuals, now became rigorously defined as the proportional survival and fecundity of a given genotype (usually simplified in scope so as to refer to all carriers of a specified pair, or pairs of alleles) relative to that genotype in the population which has the most descendants . (Unfortunately this tends to be referred to as 'Darwinian fitness' . Perhaps 'neo-Darwinian fitness' would be better, to distinguish it from Darwin's vaguer usage . ) Since the effect of any truly 'useful' feature on some life function may be assumed to contribute to the fitness of its possessors, the term adaptation, too, came to be defined by neo-Darwinians in terms of the pro­ motion or maintenance of fitness . Dobzhansky (1970), for example, cited the expression 'adaptive value' as a synonym for 'Darwinian fitness' . Or again, more recently, Ridley (1985) has stated 'Adaptation means good design for life . To understand how any particular property of an organism is adapted, it is necessary to think how it enhances its bearer's chances of survival and reproduction' . This subtle shift of emphasis in the definition from mere operational suitability to selective effect means that, in order to demonstrate adaptation, it is not good enough simply to show the effectiveness of a feature in the service of some function, however impressive that may be; it has to be shown that the feature thereby confers greater fitness on its possessors relative to alternatives . Williams (1966) further qualified this selective criterion . A given feature may accidentally benefit its possessors in special circumstances without any prior adaptation for that particular effect. For example, quick reac­ tions clearly promote the fitness of car drivers, though they obviously did not evolve by virtue of that effect . Williams considered such an 'effect' an inadequate criterion for recognizing true adap­ tation; his definition of the latter also requires evi­ dence for prior moulding of a feature by natural

selection in the service of its recognized junction(s)' . However, this creates an awkward grey area for the practical consideration of the origin of adaptations, when chance 'effects' are transformed by natural selection to established 'functions' (discussed below), and so the distinction between the two cannot always be recognized . The neo-Darwinian formulation has the effect, worrying to some, of making Darwin's charac­ terization of natural selection, 'the survival of the fittest', explicitly tautologous (as 'the survival of the survivors' ) . However, far from trivializing the theory, as might at first seem to be the case, this conclusion represents the logical outcome of purging it of teleology; selection simply acts on what organisms actually do, not what any meta­ physical agent thinks they 'ought' to do . Evolution is thus seen to be drawn in unpredictable directions by the transient effects of a myriad of immediate causes, making adaptation highly conditional . Clear illustration of this is provided by the banded snail, Cepaea nemoralis (Linne), common in parts of Britain and continental Europe . Most populations of this species are strikingly polymorphic, showing dif­ ferences in both the colour of the shell (shades of brown, pink, or yellow) and its patterning (with, or without, a variable number of longitudinal bands) . Cain and Sheppard (1954) were able to link marked differences in the relative frequencies of these variants in different habitats with preferential predation by thrushes (as estimated from broken shells around the birds' 'anvil' stones) . Effective camouflage was found to be the guiding principle, with, for example, unbanded pink and brown shells dominant in the browny leaf litter of beech woods, unbanded yellow shells on shortgrass downs, and banded yellow shells in hedgerows and longer grass . So, features adaptive in one setting were found to be demonstrably maladaptive in another, in many instances only a short distance away . Nor, indeed, can one even generalize to the extent of saying that colour and pattern, although variable, are in principle adaptive for the single broad func­ tion of camouflage; subsequent work has shown that other factors, such as response to temperature change, are of overriding importance in some per­ ipheral populations, in which different shell types acquire differing fitnesses because of their greater or lesser tendency to absorb solar heat ( Jones et al. 1977) . The intimate linkage of adaptation with natural selection raises the issue of what, precisely, natural selection acts upon, and what is thus the focus for

2 . 9 Adaptation adaptation. In cases like that of the Cepaea poly­ morphism cited above, particular variations can be attributed to the action of single gene loci (e . g . for shell colour, for presence or absence of bands, and so on) . For a given population, simple com­ binations of alleles can be assigned fitness values directly derived from, say, the live and broken shell counts . From such data one may model changes in the relative frequencies of the phenotypic variants, and thus the course of adaptation, in the population . Such exercises are the stock-in-trade of population genetics (Dobzhansky 1970) . But as Dobzhansky himself has pointed out, this apparent focus on genes as units of selection is illusory, since the fitness values assigned to them are statistical abstractions derived from the fate of those genes in many different total genotypes . Any given gene, no matter what its notional fitness value, will stand or fall according to the fate (survival and reproduction) of the genotype it finds itself in . Moreover, the phenotypic expression of any gene usually depends greatly upon interactions with other genes in the genotype and with the environment. So selection really only operates directly upon the phenotypic expression of whole genotypes . But then again, in sexually reproducing organisms, only the genes survive intact from one generation to the next . So we are here dealing with a hierarchical effect: selection on individuals in a population has the effect of altering gene frequencies in the gene pool of that population, and the latter changes in turn alter the genetic complexion of individuals in future generations, in adaptive ways . This means that adaptations, at no matter what organizational level within the individual, from the coadaptations of regulatory genes in chromosomes, through those of organelles in cells, and of tissues in organs, to the modifications of whole components of morphology, physiology and behaviour, must involve a net benefit to the individuals possessing them . The only case where this is not literally so is where there is 'kin selection' in favour of close relations, who are genetically similar if not identical . In such cases altruistic behaviour of individuals may promote their own eventual 'inclusive fitness' (effective genetic representation in future generations) through the reproductive efforts of the kin they assist, albeit at personal cost. So, for example, worker bees literally have an individual fitness of zero, being sterile, but are (painfully) well adapted to defend their genetically similar sisters due to become queens, who reproduce for them. The study of such adaptations has grown enormously from

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seminal work done in the nineteen-sixties, particu­ larly by W.D. Hamilton, and the theme is succinctly reviewed by Grafen (1984) . Other kinds of 'group selection' arguments - involving the notion of adaptations arising 'for the good of the species' require somewhat unrealistic circumstances to work, and so have found little favour with evol­ utionary biologists (Williams 1966) .

Adaptive diversity The previous section showed that in any consider­ ation of function and selection, organism and environment are inseparable . Lewontin (1983, p. 280) further stressed that ' . . . the environments of organisms are made by the organisms themselves as a consequence of their own life activities . How do I know that stones are part of the environment of thrushes? Because thrushes break snails on them. Those same stones are not part of the environment of juncos who will pass by them in their search for dry grass with which to make their nests . Organisms do not adapt to their environments; they construct them out of the bits and pieces of the external world . ' While the claim that 'organisms do not adapt to environments' is perhaps a little over­ enthusiastic, Lewontin's point about organisms defining their environment is important. The con­ stant dynamic interplay between the niche that each species so defines for itself (in Lewontin's terms) and the selection imposed on the individuals of the species by the changing constraints of that niche is one major reason for the bewildering adaptive diversity of life . Organisms of different sizes experience different environmental constraints, because of physical scaling effects, and are correspondingly diversely adapted : so, for example, the construction of an elephant has much to do with coping with gravity, while that of a pond-skater has more to do with surface tension; and bacteria (if they could think!) would probably find the notion of gravity about as abstruse as an elephant would find their experience of being jostled by molecules and ions . Then, again, there are the differences between media : stream­ lining is hardly an overriding design factor in the terrestrial mammalian carnivores, yet it is clearly a vital adaptation for their marine cousins, the seals . And even in the same circumstances, differences in habits create different experiences of the world : zebras see grass as food, and have the jaws and teeth to cope with it; lions see it as useful cover on the way to the zebras, for whom their jaws and

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teeth are suited . Adaptation breeds diversity, as Darwin rightly emphasized . Yet there is order in this diversity . The physical laws and functional specifications of habit men­ tioned above demand analogous adaptations for similar circumstances, leading to convergence: the streamlined shape of the seal is broadly repeated in other fast swimmers of similar size, such as penguins, porpoises and sharks, though with dif­ ferences in detail, of course, reflecting inherited differences in basic architecture . Moreover, the in­ herited bodyplans and the modes of growth of organisms limit the adaptive possibilities open to them. For example, gas exchange in insects takes place via branching tubes reaching into the body from spiracles along their sides . The main branches of this 'tracheal' system are ventilated tidally by contractions of the body, but in the finer tubules supplying the muscle fibres, diffusion alone suf­ fices . Muscle fibres must therefore lie close to axial tracheae, and so muscles cannot exceed a few mil­ limetres in diameter . This in turn constrains body size, the largest known insects being some Carbon­ iferous dragonflies with a wingspan not much greater than that of a crow . Considerations of such architectural constraints on evolution, and hence the mapping out of the adaptive potentialities that remain, are the business of constructional morphology (Section 4 . 1 ) .

Adaptation in palaeontology The neo-Darwinian definition of adaptation is prob­ lematical, to say the least, for palaeontologists - as the mere contemplation of trying to gauge relative survival and fecundity of genetically differing vari­ ants in fossil assemblages should suggest. However, this is not impossible . Using an ingenious argument, which deserves wider exploitation by palaeontologists, Sambol & Finks (1977) documented natural selection in a population of the Cretaceous oyster, Agerostrea mesenterica. A bulk collection from an undisturbed assemblage of their markedly plicate, arcuate shells was made from a single locality in the Maastrichtian of New Jersey, U . 5 . A . From the annual growth increments of the shells it was possible to deter­ mine the age at death of some two and a half thousand individuals . Censuses of selective mor­ tality could thus be carried out in relation to four morphometric parameters of the shells (Fig . 1 ) . The censuses showed that older individuals clustered more tightly than younger ones around mean

x

(

y

)

Fig. 1 Agerostrea mesenterica. Morphometric parameters measured by Sambol & Finks (1977) : shell arc length (AL); maximum plical height (PH); number of anterior plicae (in this case, 8); and curvature index (Y/X) . Exhalent flow would have issued around the concave posterior part of the shell .

values for the number of plicae and, with some unavoidable bias from ontogeny, for plical size as well as the overall arc length of the shell, indicating centripetal (stabilizing) selection on these features . The arcuate shape o f the shell, in contrast, was subject to differential mortality favouring maximum curvature; i . e . directed selection had operated . The features investigated all had well established functional linkages with gill suspension feeding, detected from comparisons with living oysters . In particular, the selection for increased curvature of the arcuate shell would have maximized the velocity of the exhalent current, thereby reducing the chances of recycling the processed water through the gills . This then is a clear 'snapshot' record of adaptation by natural selection in a fossil popu­ lation . As stressed by Sambol & Finks, however, the data only show the time-averaged pattern of selection on the several generations of oysters comprising the assemblage, which probably accumulated over some 200 years . Although the selection for increased curvature is consistent with the morphological trend shown by successive species of the oyster's inferred phylogenetic lineage, only a small fragment of the history of natural selection operating in this case has been sampled . Indeed, because o f the virtually insurmountable practical difficulties attached to linking longer-term evolutionary changes in the fossil record with measurable natural selection, palaeontologists have continued to use the term 'adaptation' in the sense generally adopted by Darwin, stressing functional

2 . 9 Adaptation suitability, rather than in direct reference to effects on neo-Darwinian fitness values . This distinction is important in that it lays some palaeontological per­ ceptions of adaptation open to deserved criticism . The danger is that the morphology of a fossil organism can too easily become atomized in the mind of the palaeontologist to so many discrete components, to each of which a function is imagin­ atively assigned according to the apparent suit­ ability of its morphology . The implicit assumption is that every feature must serve some function, or it would not be there . So, if one story is found wanting, another can be slipped into its place . This reductionist approach, branded as 'the adaptationist programme' , has been critized by Gould & Lewontin (1979) for proliferating adaptive hypotheses ('Just So Stories') where none may be warranted . Many features are simply the geometrical con­ sequences of the way organisms grow, and need no functional explanation per se (see also Section 4 . 1 ) . For example, any given point o n the aperture o f a Nautilus shell traces a near perfect logarithmic spiral with growth . One could devise all manner of specious arguments for how this might be 'adaptive', and the precision with which this geo­ metry is maintained might then be considered evidence for stabilizing selection . However, a brief consideration of the way the shell grows demolishes such arguments . If shell incrementation proceeds at fixed rates around the growing aperture of an expanding coiled tubular shell, logarithmic spiral growth is the geometrical consequence . That aspect of the Nautilus shell needs no adapting in order to arise, and so functional explanations for it are redundant; indeed, modification of the growth mechanism itself would be necessary to escape from such a geometry . It is thus imperative, as stressed above, always to consider the whole organism as a developing entity, in its environmental context. Bits and pieces can­ not be interpreted in isolation . Nevertheless, within that 'holistic' framework it is not only legitimate, but pragmatic to consider how particular components might have contributed to the overall conduct of an organism's life, by virtue of adaptive modification from some constructional groundplan (Mayr 1983) . Having dispensed with the erroneous re­ ductionist demand for a function for every feature, we must now ask: how is original function to be detected at all in fossil organisms (see also Section 4 . 1), and by what means can adaptation for it (in the operational sense) be diagnosed? Three steps are

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necessary: (1) from a consideration of what is known of the organism's affinities, construction, and autecology, a plausible function, or alternative functions, may be proposed for a given feature or set of features, where a constructional argument alone seems inadequate . Such hypotheses may be suggested by comparisons with similar living organisms, the design attributes of analogous machines, or even simply from theoretical con­ siderations; (2) the suitability of the feature's construction (within the constraints determined by the organism's bodyplan and mode of growth) for the proposed function must be tested . This is done by comparing it with an idealized model (paradigm) designed for that function, to see how effective the feature would be in its service; and (3), crucially for the confirmation of adaptation, evidence that the feature has indeed been modified from some dif­ ferent ancestral condition, so as to approach the form of the paradigm, must be discovered, to show that the feature in question probably did perform the function attributed to it. Testing for adaptive convergence with a paradigm really only requires an evolutionary sequence of specific modifications to be established, and this can be derived even from an outline phylogeny . There should also be reasonable evidence that the feature(s) in question consistently served the same broad function . Not all features lend themselves to such a broad-brush approach, of course, as the discussion of Cepaea polymorphism above illus­ trated. Others, however, usually concerned with such basic operational functions as feeding and loco­ motion, can be relied upon with greater confidence . A good example of such a test is Chamberlain's (1981) study of streamlining and static stability in ammonoids . Several lines of evidence suggest that the smooth-shelled ammonoids which he studied maintained the swimming habit. From an exper­ imental study of accurately constructed models he was able to draw contours of drag coefficient and static stability values on a graph of possible shell shapes, and so to identify two 'adaptive peaks' where these factors were most favourable for ef­ ficient swimming . Real ammonite data show an impressive migration to the higher of these peaks with time, providing strong circumstantial evidence for adaptation.

The origin of adaptations Ultimately, however, one is faced with the question of how an adaptation arose in the first place . Natural

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selection certainly provides a mechanism for adap­ tation once a functional effect has become apparent, but biologists can only speculate about how a feature might have become involved in this process, from comparative studies of living forms . Here palaeon­ tologists come into their own, for the fossil record furnishes the only concrete record of evolutionary history . But the virtual impossibility of charac­ terizing the role of selection in much of this means that arguments about the origins of adaptations have to be cast in terms of structural change and likely functional consequences . Two modes o f origin are conceivable : either the feature newly appeared, or it was derived from some precursor . The former implicates a 'hopeful monster' , presumably generated by some macro­ mutation. Quite apart from the vanishingly small probability of such an extreme mutation yielding a fitter genotype, the main problem with the hopeful monster model is its untestable nature . Recognition of a homologous precursor to an adapted feature, on the other hand, allows testing for functional co­ option . The point to be established is that the precursor did not originally serve the eventual function, but that with some slight modification (for whatever reason) or change in environment, ' it fort .1itously manifested effects similar to the eventual function, for which it thus became adapted . Such a precursory feature is conventionally termed a preadaptation and such, for example, would have been the grasping hands of human ancestors, for tool use, when liberated by bipedalism . Some biologists instinctively recoil from the term, believing it to smell of teleology . Its literal am­ biguousness (it might be construed, erroneously, as referring to some mysterious process of adaptive priming prior to the acquisition of a function) is a trivial problem, for which the remedy is simply learning the correct definition, with its crucial refer­ ence to fortuitous co-option . A second complaint, that it does nevertheless seem to suppose some end-directed evolution in its reference to eventual function, is a misunderstanding rooted in the essentially different working methods of many biologists and palaeontologists . Biologists investi­ gating microevolution can directly analyse pro­ cesses, but frequently stress the unpredictability of the longer term outcomes of evolution because of the myriad influences at work . Palaeontologists are in the opposite situation, knowing (some of) the outcomes of evolution, but with little direct evidence for the processes involved . The apparent 'end­ directedness' of a preadaptive hypothesis is simply

the benefit of hindsight. While the danger of sup­ posing history to have been inevitable must be avoided, it is legitimate to try to determine in retrospect at least some of the more prominent factors which made it take the unique course that it did follow. Any explanatory hypothesis must be tested against other historical models (in much the same way that Sherlock Holmes might have reconstructed the true nature of a crime) . In testing a preadaptive hypothesis, it is necessary to predict (strictly, retrodict) in detail the probable historical outcome of that model, beyond what has already been established, and to show how the retrodictions of alternative models significantly dif­ fer . Closer inspection of the fossil record can then point to one or other model being the more prob­ able, perhaps on a statistical basis . Skelton (1985) adopted this approach in testing a preadaptive hypothesis for the evolution of rudist bivalves (Fig. 2) . Constructional analysis had suggested that the spirogyrally coiled primitive forms were con­ strained by their growth geometry from exploiting the 'adaptive zones' (broad styles of adaptive morphology) occupied by their uncoiled tubular descendants . Shortening and eventual invagination of the external ligament in some spirogyrate forms had been identified as the preadaptive step which allowed the constructional changeover to uncoiled growth . The retrodiction of this model was that uncoiled taxa should have undergone an initially exponential diversification, focusing on the incep­ tion of ligamentary invagination, unmatched by their contemporaneous spirogyrate cousins . Other historical models (including a null hypothesis of random speciation and extinction) gave different retrodictions . An analysis of stratigraphical range data yielded the pattern given by the preadaptive hypothesis, at the generic level (though the species data were less enlightening, probably because of preservational bias), and this was taken to confirm the novel adaptive exploitation of the preadapted condition in the uncoiled clade .

Terminology Could and Vrba (1982) have expressed dissatis­ faction with this terminology for discussing the origin of adaptations . Noting the literal connotation of the word 'adaptation' to imply that something has been progressively 'fitted to' (ad + aptus means 'towards a fit') the execution of some function, they followed Williams (1966) in restricting the use of that term to those features which can be shown to

2 . 9 Adaptation

Fig. 2

Synoptic evolutionary history of uncoiling and its consequences in the rudists . (After Skelton 1985 . ) In primitive forms such as Diceras (lower left), the external ligament (eL) constrained the shell to grow spirogyrally, limiting its adaptive scope . Shortening and invagination of the ligament (iL) in Monopleura (centre) allowed 'uncolled' growth. Adaptive diversification ensued (e.g. clockwise from top left, Durania, Hippurites, and Pachytraga) as uncoiled taxa entered new adaptive zones.

have been shaped by natural selection for their current use . Other features, which have some useful effect by virtue of their construction, but which show no clear evidence of having been produced by natural selection through the expression of that effect, they termed exaptations ('fit (aptus) by reason of (ex)') . However, they conceded that exaptations may undergo 'secondary adaptation', so enhancing their effectiveness . As an example, they cited the useful role of the skull sutures in young mammals in aiding parturition; these are also to be found in young birds and reptiles, where they obviously have no such role to play . Together, they designated (their) adaptations and exaptations as aptations simply meaning features fitted to some function or effect. Exaptations were seen as being co-opted (,co-optation') either from pre-existing adaptations for other functions, or from constructional elements with no previous functional effect ('nonaptations') . Both constitute forms o f what has been labelled earlier, here, as 'preadaptation', though Could and Vrba criticized this term . They argued that : (1) it fails to distinguish the two kinds of exaptation, and

145

so appears to have an adaptationist bias in hinting at an earlier adaptive role for the precursory feature; and (2) it is misconstructed, implying prior fitting towards some subsequent function (the teleological odour detected by some biologists) . Time will tell if these neologisms are adopted . However, their practical value has to be queried . To deal first with the more trivial aspect of etymological correctness, if the 'fitting-to' of adaptation is simply taken to mean 'suitability for', as is the implication both in common neo-Darwinian and Darwinian (,useful variations') usage, then preadaptation literally connotes no more than 'prior suitability for' ( . . . some fortuitous functional effect) . More im­ portantly, Williams' (1966) distinction between 'effects' and 'functions' (discussed above), upon which Could and Vrba base their 'exaptations' and 'adaptations', breaks down when origin of adap­ tations is considered. In so far as any adaptation is derived from a precursory feature (whether some preadaptive trait or even a mutational novelty), then the latter must have passed through the stage of being an exaptation - i . e . exhibiting fortuitous beneficial effects - to have become subject to the selection that produced the adaptation . But the very moment that such 'exaptive' benefits were expressed, fitness would have been affected and selection would have started adapting the feature . Thus, although skull sutures are indeed 'exaptive' for mammalian parturition, the extended delay in their closing up is clearly adaptive for that process . Could and Vrba might term this a 'secondary adap­ tation', but surely this is no different from any 'primary adaptation' if we accept that all are founded on exaptations . The only reason we may choose to call one thing an exaptation and another an adap­ tation relates to the degree of modification shown . For example, it is easy to think of the skull sutures mentioned above, with the slight adaptive delay in their closure, as an exaptation, but the hooked beak of an eagle would be branded by most people as a clear adaptation for tearing flesh . Yet it is only the shape of the beak which is thus adaptive; the beak itself was, again, an exaptation for the role . In other words exaptation and adaptation are really just two aspects of the same thing, the former emphasizing derivation and the latter, destiny . To attempt to distinguish them as separate entities (which is implicit in any statement that some feature is an exaptation and not an adaptation or vice versa) seems to be as illogical as classifying the 'arrivals' and 'departures' at a railway station as two funda­ mentally different kinds of train .

146

2 The Evolutionary Process and the Fossil Record

Again, in view of the difficulties attached to de­ tecting natural selection in fossil materiat how practicable is it to attempt to distinguish between an 'exaptation' derived from a previous adaptation and one derived from a 'nonaptation'? How could one show that some feature of a fossil organism (even if dearly a product of the mode of con­ struction) did not somehow adapt the organism to its niche? The conventional toolkit of terms - adaptation and preadaptation - appear to suffice for the nature of the material to be studied, with the proviso that they are used with well understood and precisely defined (preferably explicitly stated) meanings :

Adaptation. In neo-Darwinian usage, this is a feature or complex of features in an organism which promotes or sustains the (neo-Darwinian) fitness of its possessors; or, in a palaeontological context, which has some identifiable functional effect pre­ dicted to have been of selective benefit to its pos­ sessors (a prediction which if borne out by some means of analysis would render the feature a neo­ Darwinian adaptation as well) ; or, in both cases, the associated historical process of modification of features in an evolving population .

Preadaptation . This is a feature or complex of features of an organism, whether already serving some func­ tional role or merely a constructional product, which, by virtue of its fortuitous suitability for novel functional effects, becomes co-opted as a new adaptation (in the senses given above) in descend­ ants of the organism . It should be dear that, despite the apparently simple meaning of adaptation as a vernacular term, and its fundamental importance in evolutionary theory, it actually opens onto a terminological

minefield . Safe routes across can only be picked out by adhering to dear definitions and thinking very carefully about their practical applications.

References Cain, A.J. & Sheppard, P.M. 1954. Natural selection in Cepaea. Genetics 39, 89 - 1 16. Chamberlain, J.A., Jr. 1981 . Hydromechanical design of fossil cephalopods. In: M . R House & J.R. Senior (eds) The Ammonoidea. Systematics Association Special Volume, No. 18, pp . 289 - 336 . Academic Press, London. Dobzhansky, T. 1970 . Genetics of the evolutionary process . Columbia University Press, New York. Gould, S.J. & Lewontin, R.e. 1979 . The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme. Proceedings of the Royal Society of London, B205, 581 - 598. Gould, S.]. & Vrba, E.5. 1982. Exaptation - a missing term in the science of form. Paleobiology 8, 4 - 1 5 . Grafen, A. 1984. Natural selection, kin selection and group selection. In: ] . R Krebs & N . B . Davies (eds) Behavioural ecology: an evolutionary approach, pp. 62- 84. Blackwell Scientific Publications, Oxford . Jones, J . S . , Leith, B . H . & Rawlings, P. 1977. Polymorphism in Cepaea: a problem with too many solutions? Annual Review of Ecology and Systematics 8, 109 - 143 . Lewontin, R e . 1983 . Gene, organism and environment. In: D.S. Bendall (ed . ) Evolution from molecules to men, pp. 273-285. Cambridge University Press, Cambridge . Mayr, E. 1983. How to carry out the adaptationist program? The American Naturalist 121, 324 - 334. Ridley, M. 1985 . The problems of evolution, p. 26. Oxford University Press, Oxford . Sambol, M. & Finks, R M . 1977. Natural selection in a Creta­ ceous oyster. Paleobiology 3, 1 - 16 . Skelton, P.W. 1985 . Preadaptation and evolutionary inno­ vation in rudist bivalves. In: J.e.W. Cope & P.W. Skelton (eds), Evolutionary case histories from the fossil record. Special Papers in Palaeontology No. 33, pp. 159 - 1 73 . Williams, G . e . 1966. Adaptation and natural selection - a critique of some current evolutionary thought . Prince ton University Press, Princeton .

2 . 10 Evolution of Large Size M. J . B E N T O N

body weight is proportional to volume (a three­ dimensional measure) . Thus, bone cross-sectional area has to increase relatively faster than body weight, which is why elephants and dinosaurs have legs like tree trunks (Fig . 2) . Under high stress, leg bones can buckle, or they can break without bending much . The strength of muscles also limits the size of an animal . A large animal has to be able to pull itself up from a lying position, and the heavier the animal is the more massive its muscles must be . So, muscle dimensions and muscle strength also limit the maximum size of a land animal . Locomotion is yet another limiting factor . A hypothetical animal weighing 140 tonnes could stand safely enough, but if it walked its legs would break. This is because, in walking, the force of the weight of the animal is expressed at an angle through the leg bones. Even if a giant animal could stand safely with its legs positioned vertically beneath it, it might not be able to walk because the breaking force of the bone is relatively greater . Hokkanen (1986) concluded that the heaviest pos­ sible animal able to walk on four legs would have weighed no more than 100 tonnes. The largest dinosaurs have estimated weights in the range of 80 - 140 tonnes, but the larger forms are poorly known . The 78 tonne weight of Brachiosaurus is the greatest generally accepted weight known for a terrestrial animal . The strength of bone and muscle, as described above, would have limited Brachiosaurus to a sedate walking pace of about 1 m/s with strides of only 2 . 5 m or so (quite short for an animal with 3 m legs) (Alexander 1985) . In land plants, the continuously growing supporting tissues (lignin-lined xylem cells) within a tree trunk allow vast heights and weights to be achieved . The maximum height is probably limited in part by the ability of a plant to raise sap . Water has to be 'pumped' from the ground and raised up the trunk, against the force of gravity, by means of osmosis (the sap has a higher salt content than the ground water), and the hydrostatic effect of tran­ spiration (water loss through leaves exposed to the air) . There are also mechanical constraints imposed by

Introduction Many plants and animals of the past and present are very large compared to the human scale . In particu­ lar, vertebrates, gymnosperms, and angiosperms achieved giant dimensions on occasion, and ap­ parently several times independently in each group (Table 1; Fig . 1 ) . The focus here, however, will be on truly large organisms on the human scale . The key macroevolutionary questions to be asked are : 1 Why do certain groups achieve giant size while others do not? Is it simply chance, or are there historical and mechanical reasons? 2 Why do some groups never produce giants? 3 Does evolution always go from small to large, or can it reverse? 4 How long does it take for large size to evolve in a lineage? 5 Are large organisms better adapted than small ones?

Giants and mechanical constraints The bony internal skeleton of vertebrates is ideally suited to supporting great weights in terrestrial giants . The acquisition of a fully upright posture in both dinosaurs and mammals, where the limb bones are tucked immediately beneath the body, permitted giants to evolve . The major constraints on large size in a terrestrial vertebrate are limits to the strength of bones and to the power of muscles . As animals become larger, the bones and muscles in the legs come under increasing strain, and there have to be modifications in their shape and design . Hokkanen (1986) made simple biomechanical calculations of bone and muscle strengths in order to determine the size of the largest feasible terrestrial tetrapod . Each leg bone must be strong enough to support one-quarter of the total body weight, or more if the weight is concentrated at the back, as is often the case, and there has to be a fairly large safety factor in order to allow the animal to walk or run . The strength of a bone is proportional to its cross­ sectional area (a two-dimensional measure), while

147

148

2 The Evolutionary Process and the Fossil Record

A selection of large organisms, giving some key dimensions . Fossil forms are preceded by t, and the weights quoted for these are estimates (a question mark implies that estimates are very uncertain because complete skeletons are unknown).

Table 1

Max. length (m)

Organism

Plants Algae Macrocystis, Pacific giant kelp Gymnospermophyta Sequoiadendron, Giant sequoia Pseudotsuga, Douglas fir Angiospermae Eucalyptus, Mountain ash Animals: Vertebrata Class Placodermi Dunkleosteus Class Chondrichthyes Cetorhinus, Basking shark t Carcharodon Rhincodon, Whale shark Class Reptilia Suborder Squamata Eunectes, Anaconda snake Python tKronosaurlls, Pliosaur Suborder Crocodylia t Deinosuchus Suborder Pterosauria t QlIetzalcoatlus Suborder Dinosauria t Brachiosaurus t Diplodoclls t Antarctosallrlls t 'Supersaurlls' t 'Ultrasallrus ' t 'Seismosaurlls' Class Mammalia Order Perissodactyla t Indricotherillm (= Balllchitherillm) Order Artiodactyla Giraffa, Giraffe Order Proboscidea Loxodonta, African elephant Elephas, Indian elephant Order Cetacea Balaenoptera, Blue whale Physeter, Sperm whale t Basilosallrus

Max. height (m)

Max . weight (t)

84- 1 12 126 . 5

c. 2500

60

114.3

9 10.5 13 12.6

15

0 . 23

8.4 10 15.2 16

wing span

1 1 - 12 23-27 27 30 ?24- 30 ?30- 35 ?30 - 36

11.3

0 . 09 12

?IS ?16 - 1 7

c. 6

40 - 78 18.5 80 ?75 - 1 00 ?100- 140 80+

20

5-6 7-10 6 33 . 5 20 . 7 21 . 3

the vast weight of a tall tree and the possible strength of its trunk. The weight acts vertically down the trunk, but winds can cause tremendous stresses as the crown of a tree is pushed from side to side . Experiments show that winds with speeds of 60 - 65

3-4.4 3

2-10 4 190

kmlh exert a lateral force on the tree equal to its weight (Fraser 1962) . The girth of the tree then increases in proportion to the weight (i . e . relatively more rapidly than the height increases) . At 100 m tall, a tree may be as much as 30 m in circumference

2 . 1 0 Evolution of Large Size

Fig. l

149

A selection of large animals drawn to scale . Measurements are given in Table 1. (Drawing by Elizabeth Mulqueeny. )

(Table 1), and a t much greater heights, the circum­ ference would tend to approach the height .

Why so few giants? Most other groups of organisms appear to be re­ stricted from achieving large size by mechanical and physiological constraints . For example, arthro­ pods have an external skeleton which has to be moulted frequently as the animal grows . After each moult, the animal is soft-bodied for a while, and hence vulnerable . The shed skeleton also represents a loss of body materials that have to be replaced . To achieve giant size, an arthropod would suffer the cost of moulting dozens of times . A more important constraint on large size is probably the respiratory system of tubes in the exoskeleton that allow air to

diffuse throughout the body passively . At moderate to large size, this technique would not allow all body tissues to receive an adequate supply of oxygen . There are similar constraints on large size in most other invertebrates - e . g . the respiratory system of annelids and nematodes (simple diffusion into the body); the filter-feeding habits of brachiopods, most molluscs, coelenterates, bryozoans, graptolites, and some echinoderms; and mechanical constraints of the exoskeleton of brachiopods, most molluscs, and most echinoderms . It is assumed that filter-feeding by means of exposed cilia cannot sustain a large organism. The shells of brachiopods and molluscs can reach large sizes (e .g. the giant clam, Tridacna, 1 m across), but as body size increases, shell thick­ ness has to increase in proportion to body weight to

150

2 The Evolutionary Process and the Fossil Record

Fig. 2 The pillar-like skeleton of the forelimb of A, Elephas, the Indian elephant and B, Diplodocus, a sauropod dinosaur, showing convergent graviportal (weight-bearing) adaptations : columnar arrangement of shoulder girdle (sc= scapula) and limb bones, relatively long humerus (h), large separate radius (r) and ulna (u), block-like carpal bones (c), and relatively short finger bones spreading out over a cushioning pad .

maintain the strength of the shell . The potential weight of the shell, and the amount of particulate calcium carbonate to be extracted from the seawater, tend to prevent huge size . The same is probably true for echinoids .

Cope's Rule In 1887, E . D . Cope presented a new principle of evolution, that organisms always tend towards large size. He could find no examples in which a lineage or clade of plants or animals evolved towards smaller size. Although Cope never explicitly defined this as a 'law' of evolution, it has since come to be known as Cope's Rule . In considering Cope' s Rule, many authors have focused on particular advantages of evolving large size (see below) . However, Stanley (1973) argued that Cope's Rule had general application, not be­ cause of any particular advantages of large size, but since groups tend to arise at small body size relative

to their ecological optimum. Amongst mammals, for example, the original members of most clades in the Cretaceous and Palaeocene were small carni­ vores or insectivores . On the other hand, large forms are unlikely ancestors for major new lineages since they tend to be specialized to particular habi­ tats, often by virtue of the physiological demands imposed by large size . Stanley (1973) surveyed a range of animal taxa, and found that the ancestors of a clade were generally smaller, on average, than a random sample of their descendants . Histograms of body size tended to be concentrated initially at small sizes and to be rather symmetrical . Through time, the histograms developed longer and longer tails to the right as larger body sizes arose (Fig. 3) . Size decrease also does take place in many lin­ eages, but it is rare . For example, modern horse tails and clubmosses are midgets in comparison with their Carboniferous tree-like ancestors . Certain ver­ tebrate groups have also shown reductions in size since the Pleistocene, but some of the former giants (e . g . mammoth, aurochs, giant kangaroo and wombat, giant ground sloth, glyptodon, moa) may have suffered because of human influence (see also Section 2 . 13.8).

Evolution of large size The evidence of the fossil record is that giant size can evolve very quickly in certain groups . For example, the first (small) dinosaurs of the late Triassic date from the Carnian . By mid-Norian times, 5 - 10 million years later, prosauropods such as Plateosaurus had reached body lengths of 5 m . The sauropodomorph line then achieved a length of 12 m with Melanorosaurus in the Early Jurassic, and sizes continued to increase rather slowly until the Late Jurassic when the largest known dinosaurs occurred (Table 1 ) . This last phase of size increase towards giantism - a leap from body lengths of about 12 m and weights of 10 tonnes to maxima of 30 m and 80 tonnes or more, occurred between the Bathonian and the Kimmeridgian, a time of about 20 million years . Mammals achieved large size just as rapidly, if not more so . From a maximum of cat size just before the end of the Cretaceous, rhinoceros-sized uintatheres and astrapotheres are known 10 million years later in the Late Palaeocene and Early Eocene . The largest land mammal of all time, the rhinoceros Indricotherium, was in existence by the Early Oligocene, 30 million years after the radiation began . Whales achieved large size even more

2 . 1 0 Evolution of Large Size

o

n

=

85

Pl iocene

n

=

58

Miocene

n

=

47

10

Early & Middle Eocene

12

14

Anterior - posterior length of fi rst lowe r molar ( m m )

Fig. 3

The size ranges of North American rodents - an early group, and two later groups - to show the shift from small sizes to a broad range of body sizes including many large ones. The index of size is the length of the first lower molar, which varies directly with overall body size. (After Stanley 1973.)

rapidly - the Late Eocene Basilosaurus was 21 m long, after 15-25 million years of evolution . Stanley (1979) noted that, in contrast, 'large' molluscs took much longer to evolve . The first large free-swimming clam was Megalomoidea which ap­ peared after nearly 100 million years of radiation . The first large epifaunal bivalves, the inoceramid rudists of the Jurassic and Cretaceous, took nearly 400 million years to appear . Amongst land plants, large size arose at the end of the Devonian, and especially in the Carbon­ iferous, with the first tree-like clubmosses (Lepidodendron, 45 m high) and horsetails (Calamites, 16 m high) . This had taken 50 - 60 million years of land plant evolution . Really giant gymnosperms (Sequoia and other redwoods) are known from the Jurassic, as much as 250 million years after the origin of land plants, and 150 million years after the origin of gymnosperms .

Advantages and disadvantages o f large size Numerous advantages of large size have been postulated (Stanley 1973) : improved ability to cap­ ture prey or escape from predators, greater repro­ ductive success, increased intelligence (large bodies have large brains), better stamina, expanded size range of possible food items, decreased annual

151

mortality, extended individual longevity, and in­ creased heat retention per unit volume . Protection from predation would seem to be a great advantage . Adult elephants and rhinoceroses have no regular threat from carnivores today . However, thick­ skinned mammals of the Oligocene to Pleistocene of the Northern Hemisphere and South America were subject to attacks by specially adapted sabre­ toothed cats - the Machairodontidae in North America, Europe, Africa, and Asia, and the Borhyenidae in South America. The sauropod dino­ saurs are assumed to have been immune from attack since the largest predatory dinosaurs could only have tackled very young sauropods, or dying adults . A disadvantage of large size may be greater proneness to extinction . This is not simply an attri­ bute of large size, but rather an expression of specialization . Large animals are often more re­ stricted in their niches, in their scope for adaptation, than smaller relatives . Their need for large amounts of food, or for particular environmental conditions, may make them more likely to suffer when habitats change . Also, the fact that large animals tend to have small population sizes, and hence small gene pools, makes their hold on life seem more precari­ ous . The death of a few more individuals than normal may precipitate species extinction . Bakker (1977) showed that terrestrial tetrapods surviving mass extinctions in the Late Palaeozoic and Mesozoic tended to be of small body size . Thus, the large dicynodonts and dinocephalians of the Late Permian died out, leaving smaller dicynodonts and cynodonts to cross the system boundary. A similar explanation has also been given for selec­ tivity in the Cretaceous- Tertiary event on land (Section 2 . 1 3 . 7) . In more general terms, Stanley (1979) suggested that species longevity varies with the reciprocal of body size: small species tend to survive longer than large species. This is supported by evidence from the Pliocene and Pleistocene mammalian fossil record . The only modern species that can be tracked back before 3 Ma are small mammals . All the large ones arose after that, and this is probably not an artifact of a poor fossil record since such forms are more readily fossilized than small ones . Within any clade, lineages of large organisms may be expected to display shorter taxon durations, lower rates of speciation, and higher rates of extinction (Stanley 1979), and hence greater vola­ tility in the face of environmental stress. These ideas have yet to be tested thoroughly. They are of added interest since they could be seen as charac-

152

2 The Evolutionary Process and the Fossil Record

teristics that are subject to species selection (since these are not organism-level features) . They could also potentially be interpreted as examples of the 'effect hypothesis' (Vrba 1983; see also Section 2 . 6) . This hypothesis suggests that species-level charac­ teristics, such as species duration or broad ecologi­ cal adaptation, may be incidental effects of individual characters, such as dietary or habitat preferences. Natural selection, acting on organisms, might select for large body size, which in turn might produce higher extinction rates within a lineage . These higher rates could be interpreted as an incidental effect of natural selection, rather than as a result of species-level selection . These ideas are still highly controversial .

References

some large dinosaurs . Zoological Journal of the Linnean Society 83, 1 -25. Bakker, R.T. 1977. Tetrapod mass extinctions - a model of the regulation of speciation rates and immigration by cycles of topographic diversity. In : A. Hallam (ed . ) Patterns of evolution as illustrated by the fossil record, pp. 439-468 . Elsevier, Amsterdam. Fraser, A.I. 1962. Wind tunnel studies of the forces acting on the crowns of small trees. Reports on Forest Research 1962, 178 - 1 83 . Hokkanen, ] . E . I . 1986. The size of the largest land animal . Journal of Theoretical Biology 118, 491 -499. Stanley, S . M . 1973 . An explanation for Cope's Rule . Evolution 27, 1 -26. Stanley, S.M. 1979 . Macroevolution: pattern and process . W.H. Freeman, San Francisco. Vrba, E . S . 1983. Macroevolutionary trends : new perspectives on the roles of adaptation and incidental effect. Science 221, 387-389 .

Alexander, R.McN. 1985 . Mechanics of posture and gait of

2 . 11 Rates of Evolution - Living Fossils D . C . FISHER

Introduction The study of rates of evolution encompasses a wide variety of approaches to characterization of the amount of evolutionary change within particular groups of organisms, over specified time intervals . The high level of interest that palaeontologists and evolutionary biologists have shown in this subject is not surprising, since rates are a common focus in the analysis of any process . The importance of rates, however, is often only marginally attributable to intrinsic interest in 'how rapidly' or 'how slowly' a process operates . Rather, information on rates tends to be used as a means of investigating the under­ lying dynamics of the process in question, or some­ times as input for analysing the dynamics of a related process . Much of the work on rates of evo­ lution has thus been directed toward a better under­ standing of the dynamics of evolutionary change . Studies have been designed with the intent of com­ paring rates of evolution in a variety of ways within and between particular taxonomic groups, ecological settings, and lineage geometries (e . g . ,

ancestor -descendant sequences that include lin­ eage splitting versus ones that do not) . While inter­ esting generalizations are emerging, a greater appreciation is also being gained of the difficulties of quantifying rates of evolution . 'Living fossils' i s a term frequently used t o denote extant representatives of groups of organisms that have survived with relatively little change over a long span of geological time . Such groups are im­ plicitly recognized as having displayed unusually low rates of evolution . In both professional and popular literature, living fossils collectively appear to have attracted more attention than have groups displaying unusually high rates of evolution . This may be partly because, in keeping with the inherent paradox of the term 'living fossil', evolutionary his­ tory is expected to involve conspicuous change, and it is surprising when it does not . In addition, evolutionary rate statements are commonly (though not exclusively) framed in terms of putative ances­ tor - descendant pairs, and it is easier to recognize these when the total amount of change has been small than when it has been large . Instances of

2 . 1 1 Rates of Evolution living fossils are thus more likely to be accepted on prima facie grounds than are instances of higher evolutionary rates . In any event, living fossils have frequently provided a focus for discussions of evol­ utionary rate and have helped to clarify some of the factors that may be involved in promoting or inhi­ biting evolutionary change .

Three ranges of values for evolutionary rates G . G . Simpson was one of the early major contribu­ tors to the quantitative study of evolutionary rates. He proposed that rates be classified by their abso­ lute value as 'low', 'medium', or 'high' . Although this might be considered trivial, Simpson (1944, 1953) argued that frequency distributions of evo­ lutionary rates for sufficiently inclusive sets of taxa typically contain three discrete modes, allowing low, medium and high categories to be re�ognized on non-arbitrary grounds . This empirical claim sug­ gests some degree of disjunctness in the operation of the processes and/or constraints that interact to pro­ duce evolutionary change . Simpson coined the term 'bradytely' to refer to the phenomenon of supra­ specific taxa that have shown consistently low rates of evolution . Bradytely thus encompasses the same general concept implied by 'living fossil' , but with­ out the arbitrary stipulation that a representative of the group be alive today . Simpson also suggested 'horotely' to refer to taxa comprising the middle mode in the spectrum of observed evolutionary rates and 'tachytely' to refer to supraspecific taxa showing consistently high rates of evolution . Although Simpson's (1953) demonstration of the multimodality of evolutionary rates has sub­ sequently been shown to be flawed (Gingerich 1983; Stanley 1985), the terms denoting these rate cate­ gories (especially bradytely and tachytely) have had considerable heuristic value . They are now commonly used to refer to ranges of rate values regardless of whether multimodality has been de­ monstrated independently . For instance, in a study applying the terms in this latter fashion, Raup and Marshall (1980) showed that rates within several orders of mammals were significantly higher (e . g . Cetacea and Rodentia) o r lower (e . g . Perissodactyla and Carnivora) than the mean for all mammalian orders . However, whether evolutionary rate distri­ butions (at a given rank, within some more inclusive group of organisms) tend to show some 'typical' form and, if so, whether that form is multimodal, unimodal but non-normal, or unimodal and nor­ mal, are presently open questions .

153

Qualitative categories of evolutionary rates Evolutionary rates may also be categorized by the aspect of evolutionary change that is measured. Three commonly discussed categories are genetic, morphological, and taxonomic rates . However, various subdivisions of each of these are also sig­ nificant . For instance, genetic rates include rates of DNA nucleotide substitution and rates of gene re­ arrangement, among others . These two kinds of rates refer to different processes of genetic change, acting at different levels in the hierarchy of genetic struc­ ture . Each offers its own perspective on the general phenomenon of evolutionary change, and it is con­ ceivable that each will show a different frequency distribution, even over the same large group of taxa . In the same way, morphological rates are sometimes subdivided into 'size' rates and 'shape' rates, since these two factors are commonly treated as different, though not unrelated, aspects of mor­ phology . Finally, taxonomic rates include various approaches to measurement of the longevities and rates of origination and extinction of taxa . Termi­ nology for categories of taxonomic rates varies somewhat among authors, and each category may be further subdivided according to the taxonomic rank treated . In each case, the meaning of such rates depends critically on the underlying taxonomic phil­ osophy . The type of taxonomic rate that will be focused on here is the rate of origination of new taxa of specified rank, since this corresponds most closely to a 'rate of evolution' (i . e . without intro­ ducing aspects of extinction rate) . In this categorization of evolutionary rates, gen­ etic and morphological rates refer to changes in the genotype and phenotype, respectively . An alterna­ tive convention is to distinguish between molecular and morphological rates of evolution . This retains all aspects of genotypic change within molecular evolution, but adds to it components of protein evolution that would ordinarily be considered changes in the phenotype, albeit at a molecular level. Although molecular data are usually available only for living organisms, increasing effort is being focused on extraction of some molecular data from appropriately preserved fossil material (Section 2 . 1 ) . Still, except for the success of such efforts, molecular rates can only be measured directly over relatively short timespans . Alternatively, they may be com­ puted from the cumulative divergence of contem­ poraneous taxa . In this case, some parsimony assumption is used to partition change between or among the separate lineages involved . Although

154

2 The Evolutionary Process and the Fossil Record

this approach may seem to remove molecular rates from the domain of palaeontology, we must still relate measured divergence to the time interval over which it has developed - the time since the most recent common ancestor of these taxa . Tectonic or palaeogeographical data suffice for this in certain instances, but palaeontological data provide the most commonly applicable constraints on the time of splitting of lineages . For this reason, and because of their common focus on analysis of the pattern and process of evolution, palaeontology and studies of molecular evolution are closely related (Section 2 . 1 ) . Measurements o f morphological rates may also be based on comparisons among contemporaneous taxa for which the divergence history is relatively well known . However, when morphological features can be sampled in a succession of stratigraphic intervals, we have the option of calculating rates 'directly' from the fossil record . Since any source of morphological disparity between samples will con­ tribute to perceived evolutionary rate, it is im­ portant to be aware of, and if possible control for, non-evolutionary components of variation (e . g . dif­ ferential ontogenetic representation, differential taphonomic biases, or range shifts in clinally vary­ ing populations) . If it can be argued that consecutive samples represent a series of ancestors and their descendants within a species-level lineage - an ideal situation that approximates 'tracking' mor­ phology through time - the resulting rate is referred to as a 'phyletic' rate . However, if the phylogenetic context of consecutive samples is more complex or unresolved than this, the rate is better referred to as a 'phylogenetic' rate (Raup & Stanley 1978) . Phylo­ genetic rates imply a disclaimer recognizing that increments of change may have been measured between samples that do not bear a direct ancestor ­ descendant relation to one another . Depending on the history of morphological change and the pattern of phylogenetic relationships linking consecutive samples, phylogenetic rates may be either greater or less than corresponding phyletic rates (i . e . the phyletic rates that might be measured if an arguably ancestor-descendant sequence were available) . Both of these types of rate represent transformation within a 'lineage' (broadly construed, possibly at a supraspecific level), but they differ in the degree of resolution with which the lineage can be traced . Taxonomic origination rates are likewise de­ signed to quantify change through time, but they differ fundamentally from the rates discussed thus far . To the extent that new taxa are erected to recognize some increment of morphological change

within lineages, origination rates incorporate a transformational component comparable to that as­ sessed by molecular and morphological rates . How­ ever, origination rates also include a component representing the cladogenetic (or lineage splitting) aspect of evolutionary change . The relative contri­ butions of these two components - lineage trans­ formation and lineage splitting - are difficult to quantify and rarely reported. They vary from group to group depending both on taxonomic practice and on the actual evolutionary history of the group under study .

Units of measurement for evolutionary rates Genetic or molecular rates are sometimes quantified in terms of the number of events involving a par­ ticular type of change, per time interval . Com­ parisons of molecular rates may be normalized for the number of entities 'at risk' for change (e . g . number o f nucleotide substitutions per site, per million years), but this is not practical in all in­ stances (e . g . computing the number of potential gene re arrangements ) . Molecular rates based on distance measures (e . g . DNA - DNA hybridization, immunological distance) are given in units appro­ priate to the distance measure utilized . Morphological rates may be expressed as change in the value of some morphological variable (any appropriate units of measurement), per time inter­ val . However, variables of different dimensionality (e . g . lengths versus areas) must be divided by an appropriate factor before they can be properly com­ pared . Moreover, we are usually interested in proportional rather than absolute changes in mor­ phology . Given the scaling relationships of most morphological variables (and their variances), a convenient solution is to measure morphological rates in terms of differences in the logarithm of the value of the variable of interest. A difference of a factor of e (base of natural logarithms, 2 . 718) per million years was defined by Haldane (1949) as a morphological rate of 1 darwin (d) . Rates of taxonomic origination may be measured as the number of new taxa (within a given higher taxon) per time interval . This is often expressed as a percentage increase, normalized for the length of the time interval . Rate of origination may also be calculated from the rate of change in total diversity at a given taxonomic level and the rate of extinction at that level. In interpreting origination rates, it is important to consider such possible complications as differential effects of taphonomic and mono-

2 . 1 1 Rates of Evolution graphic biases, and differential application of taxo­ nomic practice within and between groups being compared (Raup & Marshall 1980) . From an evo­ lutionary standpoint, however, a more fundamental issue with rates of taxonomic origination is that they lump together information on lineage trans­ formation and lineage splitting . Given the current unevenness of our detailed phylogenetic knowledge of most groups, this may be an unavoidable com­ promise, and indeed, it offers some benefits of convenience and succinctness in the representation of evolutionary history . However, it is to be hoped that more phylogenetically discriminating ap­ proaches to studying diversification will be developed in the future .

The effect of measurement interval on evolutionary rates Measured rates are commonly treated as indepen­ dent of the interval length over which they are measured. For processes occurring at approximately constant rates, this characterization is acceptable . However, for any variable-rate process, the measured rate is an average and may be influenced strongly by rate fluctuations during the measure­ ment interval . Depending on the temporal structure of rate fluctuations and the range of intervals being considered, measured rates will be more or less susceptible to biasing effects from interval length . Some molecular rates appear to behave in 'stochastically constant' fashion, at least over certain time-spans (commonly of the order of tens of millions of years) . The relative constancy of these rates (with both rate and constancy varying from one molecular system to another) has led to the proposal of the 'molecular clock' hypothesis (see also Section 2 . 1 ) . According t o this hypothesis, molecular difference, once calibrated to reflect rate of change, can be used as a measure of time since lineage divergence (Fitch 1976) . However, even for molecular clocks that are relatively 'well behaved' over a particular time inter­ val within a given group, there is growing evidence that observable change has either accelerated or decelerated at other times during the history of that group (Goodman et al. 1982; Gingerich 1986) . For divergence times that span periods of significant rate change, systematic biases can be anticipated . The factors thought to influence morphological rates (see below) are known to fluctuate on a variety of time-scales . Because neither the highest nor the lowest rates are likely to be maintained over pro­ tracted periods of time, the largest range of variation

155

should be observed in comparing rates measured over the shortest time intervals . For the same reason, there should be a tendency toward intermediate values, which are due to averaging of rate fluctu­ ations, when measuring over longer intervals . Since morphological rates are typically expressed in terms of net change in the value of some morphological variable, changes in the direction of morphological change, as well as in the rate of change per se, contribute to the moderation of rates measured over longer time intervals . This interaction is partly responsible for the decline in maximum observed morphological rates with increasing measurement interval (Fig . 1) . However, as Gingerich (1983) pointed out, the lower, and to some extent the upper bounds of the distribution of observed rates in Fig . 1B are also influenced by factors unrelated to evolutionary process . The lower bound corresponds to a practical limit of measurement precision, beyond which earlier and later forms would not usually be recognized as different, yielding a rate of zero . The upper bound, on the other hand, rep­ resents an effective limit beyond which pairs of earlier and later forms differ so strongly that their relationship, and hence their appropriateness for a rate calculation, is likely to be questioned . The result is a tendency for longer measurement inter­ vals to yield lower rates . Because of these biasing factors, comparison of rates measured over very different time intervals is a non-trivial problem . Many comparative studies of evolutionary rates have not adequately dealt with this issue . Taxonomic rates are also affected by measurement interval, but not in all the ways noted above . As with morphological rates, rates of origination cal­ culated over longer intervals are likely to be damped by averaging a range of shorter-term values . How­ ever, rates of origination are not moderated by changes in the 'direction' of evolution; 'new taxa' are new taxa, even if they show reversals in certain attributes . In addition, with rates of origination, low values do not suffer an interval-related bias based on measurement precision, nor do high values necessarily engender suspicion of lack of relationship .

The effect of stratigraphic completeness on evolutionary rates Stratigraphic completeness (see also Section 3 . 12) could in principle affect the precision of palaeon­ tologically documented divergence times, but in practice, phylogenetic uncertainties and disconti-

2 The Evolutionary Process and the Fossil Record

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Fig. 1 Inverse relationship between morphological rates of evolution and the time intervals over which they are measured (after Gingerich 1983), illustrating some of the biasing effects discussed in the text. A, Subset of rates shown in B, plotted on linear axes. B, Logarithmic transformation of rate distribution; time intervals range from 1 . 5 to 350 million years. Rates plotted in domain I (open squares) represent laboratory selection experiments; domain 11 (open circles, and digits for multiple cases; X > 9) represents historical colonization events; domain III (digits) represents post-Pleistocene events; and domain IV (digits) is drawn from the pre-Holocene record of invertebrates and vertebrates .

nuities i n the preserved record o f taxa (even within intervals that have a sedimentary record) are more important sources of error in these estimates . Stratigraphic completeness increases in importance, however, when morphological or taxonomic rates read 'directly' from the fossil record are considered . I n a relatively incomplete section, the actual age difference between two samples may be either much greater or much smaller than their estimated age difference based on linear interpolation from dated levels. This translates into substantial im­ precision in rate measurements . In order to mini­ mize this problem, Dingus & Sadler (1982) suggested that rates only be measured at levels of resolution for which stratigraphic sections can be considered complete (i . e . for which each included interval of given magnitude is likely to be rep­ resented by sediment) . Following this recommen­ dation, relatively incomplete sections limit us to longer time intervals for rate measurement and thus, through the biasing effect of interval length, tend to yield lower rates than might be seen in more complete sections . Relatively incomplete sections also tend to reduce measured rates of origination .

Factors affecting actual rates of evolution Having explored some of the factors that tend to distort perceptions of evolutionary rates, the sources of real variation in such rates will now be discussed . Among the more conspicuous of these are controls of the rate of transformation within established, species-level lineages. These include : mutation rate; generation time; degree of resource specialization; and the nature, amount, and distribution of varia­ bility within populations . Population size may also be important but is probably overshadowed by population structure - the pattern and scale of subdivision of populations and the degree of re­ productive interaction between those subdivisions . Other factors are a t least partly extrinsic t o the species in question : rate of environmental change; ecological factors such as the level of interspecific competition; and, in general, the intensity of selec­ tion (assuming selection and fitness are defined so that intensity of selection is not trivially equivalent to rate of evolution) . Another group of controls overlaps somewhat with the first but may be distinguished as operating at a different level in the genealogical hierarchy . It

2 . 1 1 Rates of Evolution

157

consists of factors that determine the rate of in­ itiation of new species-level lineages . Speciation rate assumes particular importance in a punctuated view of evolution, but its role in influencing evo­ lutionary rate is not dependent on the predominance of a punctuated mode of evolutionary change . In­ trinsic controls on speciation rate include such factors as dispersal ability (also relevant as a deter­ minant of population structure) and degree of resource specialization . There are also extrinsic con­ trols, such as rate or incidence of habitat fragmen­ tation by geomorphic or tectonic processes.

Living fossils - alternative definitions Living fossils figure in discussions of evolutionary rates as a conspicuous and yet potentially tractable case in which the relationship between a large-scale evolutionary pattern and its underlying causes may be explored (Eldredge & Stanley 1984; Schopf 1984) . As noted above, the central concept in the definition of living fossils is survival over long periods of time with minimal morphological change . Auxiliary cri­ teria have been appended by various authors and do indeed apply to certain cases traditionally recognized as living fossils . However, they are much less applicable to others . For instance, a relict geo­ graphical distribution and greatly diminished pre­ sent (relative to past) diversity characterize Sphenodon (a rhynchocephalian) and Nautilus (a nautiloid cephalopod), but not Limulus and related genera (horseshoe crabs) . Likewise, Latimeria (a coelacanth) and Neopilina (a monoplacophoran) rep­ resent clades once thought to be extinct, but Lepisosteus (a gar) and Lingula (an inarticulate brachiopod) have long been known from both fossil and Recent biotas . Living fossils are some­ times referred to as 'species' that have persisted for inordinately long periods of time, but few if any instances are actually founded on well docu­ mented species-level identity. The most generally useful definition therefore focuses on supra specific taxa that have shown unusual morphological conservatism . One of the most commonly cited living fossil groups is the Xiphosurida, or horseshoe crabs . Fig . 2 provides some sense of the morphological conservatism that can be seen within this group, comparing the extant species Limulus polyphemus with the Triassic Limulus vicensis . While the generic identity of these two species may be questioned (Fisher in Eldredge & Stanley 1984), their overall anatomical similarity is evident . Other species with-

Fig. 2 Horseshoe crabs, a commonly cited living fossil group . A, Dorsal aspect of a juvenile Limulus polyphemus, Recent, distributed along much of the eastern coast of North America; c. one half actual size. B, Dorsal aspect of a specimen of Limulus vicensis, Triassic, France; c. actual size . The tail spine is not preserved on this specimen, but it was presumably present originally. (From Bleicher 1897.)

158

2 The Evolutionary Process and the Fossil Record

in the group show greater morphological diver­ gence, but the reputation for bradytely has focused on comparisons such as that given here .

B RADYT E LY

TAC H YT E LY

Bradytely - alternative explanations The problem posed by living fossils is to explain the general phenomenon of bradytely . Simpson's (1944, 1953) interpretation was that the low rates of long­ term morphological evolution shown by bradytelic lineages are a consequence of unusually low rates of intraspecific phyletic transformation (Fig . 3A) . This appears to be a testable proposition, but it has thus far received little direct, empirical evaluation (per­ haps because few bradytelic groups have a suf­ ficiently continuous fossil record) . However, some of the factors that have been suggested as respon­ sible for low rates of phyletic transformation (e . g . unusually low levels o f morphological o r genetic variability) have been assessed within bradytelic groups and found not to differ significantly from values typical of nonbradytelic taxa (e . g . Selander et al. 1970) . Other factors that could in principle be responsible (e . g . extreme habitat stability, or strongly canalized development) are difficult to test. Some factors do seem to hold for a wide range of bradytelic groups and have been thought to contrib­ ute directly to low rates of intraspecific change (e . g . ecological generalization and broad physio­ logical tolerance; Simpson 1953) . Nevertheless, consideration of alternative explanations is clearly warranted . Another approach to interpreting bradytely steps up a level in the hierarchy of evolutionary pro­ cesses - from intraspecific interactions to the circumstances surrounding speciation events (cladogenesis) . It depends, furthermore, on the proposition (associated with the concept of punc­ tuated equilibrium) that most morphological change is accomplished during and driven by cladogenesis, and that the subsequent history of species tends to be dominated by morphological stasis . Under this characterization of evolution, a low rate of intra­ specific transformation would be the norm and would not be seen as a sufficient cause of bradytely . However, bradytely might be due to unusually low rates of speciation within bradytelic lineages (Fig. 3B); according to this interpretation, low speciation rate would allow few opportunities for morphologi­ cal change and would thus restrict a lineage to a relatively low rate of change averaged over the long term (Eldredge 1979) . As long as speciation is understood as a process that is not itself dependent

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Schematic representation of three explanations of controls on long-term rate of morphological evolution. (After Fisher in Eldredge & Stanley 1984.) A, The contrast between bradytely and tachytely may be due to differences in the rate of intraspecific morphological transformation. B, The same contrast may be due to differences in rate of speciation. C, Bradytely and tachytely may also reflect higher-order patterns of differential survival and cladogenesis .

on morphological change, this interpretation represents a novel perspective on bradytely . Yet there is still a question as to why certain taxa, retrospectively recognized as bradytelic, show such a low rate of speciation . One possible answer has been suggested by the observation that a number of bradytelic taxa also show tendencies toward eurytopy - i . e . they have, at least in many respects, relatively broad, generalized ecological require­ ments . In this, they contrast with stenotopic taxa, which have relatively narrow, specialized require­ ments . It has been suggested that, relative to stenotopic taxa, eurytopic taxa are less subject to di­ rectional selection, often have broader geographical

2 . 11

Rates of Evolution

ranges, and tend to have populations that are less susceptible to range disruption and consequent reproductive isolation Gackson 1974; Eldredge 1979; Vrba in Eldredge & Stanley 1984) . This may result in a lower rate of speciation and a lower likelihood of morphological divergence during speciation . The case studies of bradytely in Eldredge & Stanley's (1984) compendium offer qualified support for the association of bradytely, low speciation rate, and eurytopy, but rigorous evaluation of this pattern is difficult because of the lack of quantitative indices of morphological conservatism or eurytopy . In addition, measurements of speciation rate are sub­ ject to significant sampling problems, such that even an evaluation of the relationship between speciation rate and subjective assessments of bradytely and eurytopy would be complicated . A third interpretation o f bradytely i s that i t arises at an even higher level in the genealogical hierarchy, as a result of differential survival of relatively primitive and relatively derived lineages within a clade (Fig . 3C) . Treated simply as a phylogenetic pattern, bradytely may or may not have any single lower-level cause, but whether it does or not, it could be independent of any systematic difference in intra specific rates of transformation or rates of speciation (Fisher in Eldredge & Stanley 1984) . While any of these three explanations of bradytely might operate in isolation from the others, they are not mutually incompatible . Nor can the possibility be ruled out that different instances of bradytely are traceable to different mixes of factors operating at a variety of levels . Although there are thus no simple answers, the investigation of bradytely has led to an expanded appreciation of the possible controls of long-term evolutionary rates.

159

References Bleicher, M. 1897. Sur la decouverte d'une nouvelle espece de limule dans les marnes irisees de Lorraine. Bulletin des Seances de la Societe des Sciences de Nancy 14, 116- 126 . Dingus, L. & Sadler, P. M. 1982. The effects o f stratigraphic completeness on estimates of evolutionary rates. System­ atic Zoology 31 , 400-412. Eldredge, N . 1979 . Alternative approaches to evolutionary theory. Bulletin of the Carnegie Museum of Natural History 13 , 7 - 1 9 . Eldredge, N. & Stanley, S.M. (eds) 1984 . Living fossils . Springer-Verlag, New York. Fitch, W.M. 1976 . Molecular evolutionary clocks. In: F.J. Ayala (ed .) Molecular evolution . Sinauer, Sunderland, Mass . Gingerich, P.D. 1983 . Rates of evolution: effects of time and temporal scaling . Science 222, 159 - 1 61 . Gingerich, P.D. 1986. Temporal scaling of molecular evolution in primates and other mammals. Molecular Biology and Evolution 3, 205 - 221 . Goodman, M . , Weiss, M . L . & Czelusniak, J. 1982. Molecular evolution above the species level : branching pattern, rates, and mechanisms . Systematic Zoology 3 1 , 376-399. Haldane, J . B . 5 . 1949 . Suggestions as to quantitative measurement of rates of evolution. Evolution 3, 5 1 - 56. Jackson, J.B.C. 1974. Biogeographic consequences of eurytopy and stenotopy among marine bivalves and their evo­ lutionary significance . American Naturalist 108, 541 - 560. Raup, D.M. & Marshall, L . G . 1980 . Variation between groups in evolutionary rates: a statistical test of significance . Paleobiology 6, 9 - 23. Raup, D.M. & Stanley, S.M. 1978. Principles of paleontology, 2nd edn . Freeman, San Francisco . Schopf, T.J.M. 1984. Rates of evolution and the notion of living fossils. Annual Review of Earth and Planetary Sciences 12, 245-292. Selander, R.K., Yang, S . Y . , Lewontin, R. c . & Johnson, W.E. 1970 . Genetic variation in the horseshoe crab (Limulus polyphemus), a phylogenetic "relic" . Evolution 24, 402-414. Simpson, G.G. 1944. Tempo and mode in evolution . Columbia University Press, New York. Simpson, G . G . 1953 . The major features of evolution . Columbia University Press, New York. Stanley, S.M. 1985 . Rates of evolution. Paleobiology 11, 13-26 .

2 . 12 Mass Extinction: Processes were destroyed in the Late Devonian (Section 2 . 1 3 . 3) and end-Triassic (Section 2 . 1 3 . 5) episodes and the calcareous plankton (foraminifera and coccolitho­ phorids) drastically reduced at the end of the Cretaceous (Section 2 . 1 3 . 6) . The biggest event of all was at the end of the Permian (Section 2 . 13.4), when many important Palaeozoic groups went completely extinct, including fusulinid foraminifera, came rate and inadunate crinoids, trepostome and crypto­ stome bryozoans, rugose corals, and productid brachiopods . All but the first of these extinction episodes have subsequently been accepted by palaeontologists as the most significant extinction events in Phanerozoic history (Raup & Jablonski 1986) . The correlation between major sea-level falls and Newell's mass extinction events is indeed striking (Fig . 1; Jablonski 1986) . On a smaller scale, there is an equally striking correlation between the extinction of environmentally sensitive groups such as am­ monoids and other episodes of widespread re­ gression, probably correlating with sea-level fall, in both the Palaeozoic and Mesozoic (e . g . Hallam 1987a) . Following ecological research on island bio­ geography, it is clear that smaller habitat areas can accommodate fewer taxa, so reduction in area must lead to lower diversity as the extinction rate in­ creases . Whether the extinction is due to reduced habitat diversity, increased competition, crowding effects, or whatever, the basic empirical relation­ ship appears to be well established . Critics have pointed out that inferred episodes of significant marine regression do not always correlate with notable mass extinctions of marine organisms . This is most obviously true for eustatic falls of sea­ level in the Quaternary and Middle Oligocene, the latter being probably the largest in the Tertiary (Haq et al. 1987) . At least two explanations can be put forward, both of which take into account the phenomenon of biological adaptation. Quaternary regressions were followed by equally rapid trans­ gressions after geologically short time intervals, limiting the effect of reduced habitat area and per­ mitting a sufficient number of organisms to survive and expand their populations during the succeeding transgressions . Quaternary faunas are likely to have been relatively eurytopic, or environmentally toler­ ant, because they represent survivors of environ­ mentally stressful Late Cenozoic times . The same

2 . 12 . 1 Earth-bound Causes A . H A L L AM

Introduction The idea that mass extinctions could be caused by strictly Earth-bound phenomena is an old one, dating back to the so-called heroic age of geology in the early part of the nineteenth century . Following the pioneering extinctions research of his compatriot G . Cuvier, the French geologist Elie d e Beaumont pro­ posed that catastrophic, virtually instantaneous upheavals of mountain ranges at infrequent inter­ vals through geological history caused drastic envi­ ronmental changes leading to the destruction of a high proportion of the Earth' s biota . The correlation between episodes of diastrophism and times of major organic turnover was also noted by the American geologist T . e . Chamberlin at the begin­ ning of this century, and by European geologists such as E. Suess and J . F . Umbgrove (Hallam 1981a) . Modern research on tectonic activity suggests, how­ ever, that it is too localized geographically and insufficiently 'catastrophic' in time to account satis­ factorily for mass extinction events . Attention must be confined to phenomena global in scale that can give rise to drastic changes in the physical environ­ ment . The only plausible contenders are changes in sea level and climate, and episodes of increased volcanicity.

Sea-level The American palaeontologist Newell (1967) was the first person to make an explicit correlation be­ tween mass extinction episodes among Phanerozoic marine invertebrates and eustatic falls in sea-level, attributing the extinctions to increased environ­ mental stress consequent upon substantial re­ duction of habitat area of shallow epicontinental seas. He distinguished six such episodes : end­ Cambrian, end-Ordovician, Late Devonian, end­ Permian, end-Triassic and end-Cretaceous . The first two are especially well marked by trilobite extinc­ tions and the last three by ammonite extinctions . Extensive communities o f reef-dwelling organisms

160

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consideration may apply also to the Middle Oligocene regression, which followed closely on a significant increase in marine extinction rates across the Eocene - Oligocene boundary . It is likely that for long periods of Phanerozoic time most organisms became so well adapted to conditions of relative environmental stability, including equable climate, that even modest changes of sea-level could have had a striking effect on so-called 'perched faunas' in extensive and extremely shallow epicontinental seas . Such palaeogeographic phenomena cannot be closely matched at the present day, which marks an unusually regressive episode in Earth's history. The latest Exxon sea-level curve from the Triassic

161

to the present (Haq et al. 1987) does not show unusually large falls at the times of the two greatest marine extinction episodes during this interval, the end of the Triassic and the end of the Cretaceous . The Exxon curve is based largely, however, on seismic stratigraphy, and should not be treated as more than a tentative model to be subjected to testing by other evidence . There is indeed con­ siderable evidence of a major end-Triassic regression (Hallam 1981b), and some strong indi­ cations that the extent of the end-Cretaceous re­ gression has been underestimated by Haq et al. (Hallam 1987b) . For several events, namely the end-Permian, end­ Triassic and end-Cretaceous, mass extinctions in the marine realm appear to correlate closely with mass extinction of some terrestrial vertebrates, notably those large in size, which, because of their relatively low population numbers and reproductive rates, would be more vulnerable to environmental disturbance than smaller organisms (see also Section 2 . 10) . Obviously such extinctions cannot be ac­ counted for by reduction in land area, and a more likely explanation is bound up with the increased continental seasonal temperature contrasts induced by regression of epicontinental seas . While much attention has been paid to regression as a promoter of extinctions it should be noted that there is a strong association between inferred sea­ level rises that follow directly after falls and the spread of anoxic water in epicontinental seas, as recorded for instance by widespread laminated black shales . Habitable areas can be as severely reduced by this means as by regression, with a mass extinction event ensuing . For many extinction events, both major and minor, a clear correlation exists with extensive deposits of black shales . Among the major events the best examples are the basal Silurian and basal Famennian (Devonian), effectively equivalent to the end-Ordovician (Sec­ tion 2 . 1 3 . 2) and end-Frasnian (Section 2 . 13.3) ex­ tinction events . Among minor events the clearest examples are the Cenomanian- Turonian boundary and Early Toarcian (Hallam 1987a) . The spread of anoxic bottom waters may possibly also be impli­ cated as a contributory factor in the end-Permian (Section 2 . 13.4) and end-Triassic (Section 2 . 13 . 5) events . For much of Phanerozoic history the ocean might have been poorly stratified, in marked contrast to the present-day situation (Wilde & Berry 1984) . In consequence the deeper ocean would be more or less anoxic and could not have served as a refuge for

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2 The Evolutionary Process and the Fossil Record

shallow-water organisms at times of regression, or if they were outcompeted by other organisms . It is more than possible that the great bulk of the modern deep-sea fauna, which contains representatives of most phyla, is no older than Tertiary . Since the Late Eocene there has evidently been a system of strong currents induced by Antarctic glaciation, which have served to aerate bottom water in the deep ocean (Hallam 1981a) . Lack of a deep water anoxic zone could help to explain why there is no signifi­ cant extinction recorded for the major Middle Oligocene regression . The cause of sea-level changes is bound up either with the melting and freezing of polar icecaps or with tectonics, such as the uplift and subsidence of ocean ridges and the splitting or collision of conti­ nents . The end-Ordovician event might well have had a glacioeustatic cause, associated with growth and disappearance of the Saharan ice sheet, but for the other major extinction events the most likely cause is tectonoeustatic . This poses a problem, be­ cause the rates of sea-level rise and fall produced by plate tectonics are approximately three orders of magnitude lower than for glacioeustasy, thereby allowing more time for organisms to adjust to a changed environment and hence avoid extinction . Unfortunately there are as yet insufficient data from the strati graphic record, on amount and rate of sea­ level change, to resolve this problem satisfactorily . There remains another possibility, that rapid re­ gressions and transgressions on a regional rather than a global scale could be produced as a result either of changes in the pattern of lateral stresses in the crust (Cloetingh et al. 1985) or by the rise of mantle plumes to cause epeirogenic uplift, with related volcanism associated with subsidence (Loper & McCartney 1986) . The fact that such changes would not strictly come under the category of eustatic is irrelevant as far as the organisms are concerned, provided that the changes in question are both geographically extensive and rapid, thereby leading to drastic changes in the environment .

Climate Changes of sea-level could have, as a by-product, some climatic consequences, but climate could of course fluctuate with time independent of eustasy . Stanley (1984, 1987) has been the strongest advocate of the view that temperature changes in the marine realm have been the dominant causal factor in Phanerozoic mass extinctions . This interpretation involves a gross extrapolation from his detailed

studies of Plio-Pleistocene molluscan extinctions off the Atlantic and Gulf coasts of the U . S . A . Whereas there is a high rate of species extinctions in this region, there is negligible evidence of contemporary extinctions around the Pacific margins, or the Mediterranean . Stanley maintained that, because the extinctions are regional not global in extent, eustatic changes cannot be invoked . Instead he argued for a more pronounced lowering of tempera­ ture on the American east coast than elsewhere, as a result of palaeogeographical factors . Extending back through time, the next major marine extinction event for which temperature decline can plausibly be invoked is across the Eocene - Oligocene boundary . This 'event' is de­ cidedly not sudden in geological terms and is marked more by a pronounced increase in extinction rate rather than a drastic change over a narrow time interval . There is good independent evidence from oxygen isotopes of a fall in both surface and bottom water temperatures, but no indication from the curve of Haq et al. (1987) of sea-level changes sig­ nificantly larger than at other times in the Tertiary . For pre-Tertiary times, however, the evidence im­ plicating temperature as a causal factor is weak to non-existent, forcing Stanley to resort to some special pleading (though it could be argued that the end-Ordovician event (Section 2 . 13.2) had an ulti­ mate climatic causation, if the glacioeustatic in­ terpretation is accepted) . For example, the largest extinction event of all, at the end of the Permian (Section 2 . 1 3 .4), took place during a period of clima­ tic amelioration, marked by the Middle Permian disappearance of the Gondwana ice sheet. It is con­ ceivable, of course, that the end-Permian event was induced by an episode of temperature rise, but no plausible case has been made for this . One of the points that Stanley cited in favour of his temperature control hypothesis is that the most extinction-vulnerable organisms, such as reef dwellers, were tropical in distribution throughout Phanerozoic history . While this may be true, it does not necessarily establish temperature as the key control, because tropical organisms tend to be gen­ erally stenotopic, as they are relatively sensitive to a variety of environmental factors . A really extensive overturn of deep anoxic water at the beginning of episodes of climatic change has been suggested as a possible contributing factor to mass extinction events in the oceans (Wilde & Berry 1984) . As discussed above, the rise and spread onto continental shelves of anoxic water is often associ­ ated with marine transgressions, so that it may be

2 . 1 2 Mass Extinction : Processes unnecessary to invoke climatic change as well . As regards changes in air temperature, the only satisfactory record comes from Late Cretaceous to Recent terrestrial plants . No striking extinction event has been recorded among these organisms for the Cenozoic, but at the end of the Cretaceous there were significant extinctions in the North Temperate Realm of western North America and Eastern Asia . Whereas the palaeobotanical consensus has related such extinctions to gradual temperature decline through the Late Cretaceous, the most recent re­ search in the North American Western Interior suggests a temperature rise in the Maastrichtian and no significant change across the Cretaceous ­ Tertiary boundary (Wolfe & Upchurch 1987) . Further back in time the evidence from terrestrial plants is more obscure, and has so far not been adequate to establish a convincing picture of climatic change .

Volcanism The end-Cretaceous extinction event is the one that has received by far the most attention (see also Sections 2 . 1 3 . 6, 2 . 1 3 . 7) . Notwithstanding the claims made for extra-terrestrial impact, there is strong evidence for marine regression at this time, suggesting that this phenomenon is involved in the extinctions . Sea-level change cannot account, how­ ever, for the drastic extinctions at the Cretaceous ­ Tertiary boundary of calcareous plankton, nor for such physico-chemical evidence as an anomalous enrichment on a global scale of iridium, and the presence locally of quartz grains with shock­ metamorphic laminae, in Cretaceous-Tertiary boundary layers (see also Section 2 . 12.2) . Evidence of this sort has been claimed as conclusive for bolide impact, but in fact a case of at least equal plausibility can be made for terrestrial volcanism on a massive scale (Hallam 1987b) . It is known that aerosols enormously enriched in iridium compared with crustal rocks can be expelled from the mantle during flood basalt eruptions . Eruptions of this kind on a sufficient scale over several 100 000 years could produce the observed global enrichment of the element . The Deccan Traps of India, erupted during the magnetic zone that embraces the Cretaceous -Tertiary boundary, are the most ob­ vious candidate . There is good evidence of contem­ porary explosive volcanism in other parts of the world, and reasonable grounds for believing that such volcanism can generate the pressures required to produce shock-metamorphic laminae in mineral grains.

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Massive volcanism over an extended period would have deleterious environmental conse­ quences . It is known that flood basalt fissure erup­ tions that produce individual lava flows with volumes greater than 100 km3 at very high mass eruption rates are capable of injecting large quan­ tities of sulphate aerosols into the lower strato­ sphere, with potentially devastating atmospheric consequences . Such volatile emissions on a large enough scale would lead to the production of im­ mense amounts of acid rain, reduction in alkalinity and pH of the surface ocean, global atmospheric cooling, and ozone layer depletion . Atmospheric cooling would be reinforced by ash expelled into the atmosphere by contemporary explosive volcanicity . Thus for the end-Cretaceous extinctions a com­ pound scenario seems to be required, involving both sea-level fall and volcanicity on an exception­ ally intense scale, with associated climatic changes (there is as yet, however, no evidence to support the notion that volcanicity was a direct causal factor for other mass extinction events) . Loper and McCartney (1986) noted that increased end-Cretaceous volcan­ ism correlates with a significant change in the geo­ magnetic field, with a long Cretaceous reversal­ free period coming to an abrupt end in the Maastrichtian. They proposed a model involving periodic instability of the thermal boundary layer at the base of the mantle . This layer accepts heat from the core and transmits it upward by way of mantle plumes. As it thickens by thermal diffusion it be­ comes dynamically unstable and hot material erupts from it. Heat is extracted from the core at a greater rate, increasing the energy supply and hence the magnetic reversal frequency of the dynamo in the fluid outer core . Hot material rises through mantle plumes to the surface to give rise to volcanic activity . Both non-explosive and explosive volcanism can be produced, depending on the condition of the litho­ sphere, which varies regionally . Increased mantle plume activity has the potential for causing uplift of extensive sectors of continents and hence regression of epicontinental seas . Present-day hotspots are as­ sociated with regional topographic bulges, so it is reasonable to infer that most epeirogenic uplifts reflect hot, low density regions in the astheno­ sphere, derived from plume convection . Epeirogenic subsidence on the continents and marine trans­ gression might be expected to follow episodes of substantial volcanic eruptions . Fischer (1984) put forward a general hypothesis that relates changes of sea-level, climate, and volcan-

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icity to produce two supercycles during Phanerozoic time . Times of high rates of ocean floor spreading and oceanic volcanicity correlate with buoyant ocean ridges and consequently high sea-level stands . Less carbon dioxide is removed from the atmosphere by terrestrial weathering because of reduced continental area, and the volcanicity brings more of the gas to the Earth's surface . Thus the carbon dioxide content of the atmosphere is high, and because of the greenhouse effect the climate is equable, with no polar ice caps . The converse tec­ tonic situation gives rise to low sea-level stands, low atmospheric carbon dioxide, and stronger climatic differentiation between the tropics and the poles. The rates of change involved in such processes appear, however, to be too low to account for mass extinction events . The most promising line of ap­ proach in generating terrestrial models is probably a closer investigation of the relationship between sea-level change, continental uplift, volcanism, and mantle plume activity, as has been proposed for events across the Cretaceous - Tertiary boundary (Sections 2 . 1 3 . 6, 2 . 1 3 . 7) . The end-Permian extinction episode (Section 2 . 13 .4) is an especially promising candidate for this type of investigation.

References Cloetingh, S . , McQueen, H . & Lambeck, K. 1985 . On a tectonic mechanism for regional sea level variation. Earth and Planetary Science Letters 75, 157- 166. Fischer, A.C. 1984 . The two Phanerozoic supercycles . In: W.A. Berggren & J . A . van Couvering (eds) Catastrophes and Earth history, pp. 129 - 150. Princeton University Press, Princeton. Hallam, A. 1981a. Facies interpretation and the stratigraphic record. W.H. Freeman, Oxford . Hallam, A. 1981b . The end-Triassic bivalve extinction event. Palaeogeography, PalaeoC/imatology, Palaeoecology 35, 1 -44. Hallam, A. 1984. Pre-Quaternary sea-level cha�lges. Annual Review of Earth and Planetary Sciences 12, 205- 243 . Hallam, A. 1987a . Radiations and extinction in relation to environmental change in the marine Lower Jurassic of northwest Europe . Paleobiology 13, 152 - 1 68. Hallam, A. 1987b . End-Cretaceous mass extinction event: argument for terrestrial causation . Science 238, 1237-1242. Haq, B . U . , Hardenbol, J . & Vail, P.R. 1987. Chronology of fluctuating sea levels since the Triassic . Science 235, 1 1 58- 1 167. Jablonski, D . 1986 . Causes and consequences of mass extinc­ tions . In: D.K. Elliott (ed . ) Dynamics of extinction, pp. 183-229 . Wiley, New York . Loper, D . E . & McCartney, K. 1986. Mantle plumes and the periodicity of magnetic field reversals . Geophysical Research Letters 13, 1525 - 1528. Newell, N.D. 1967. Revolutions in the history of life . Special Papers of the Geological Society of America 89, 63-91 .

Raup, D . M . & Jablonski, D. (eds) 1986 . Patterns and processes in the history of life. Report of Dahlem Workshop, 1985 . Springer-Verlag, Berlin, Heidelberg. Stanley, S.M. 1984. Marine mass extinction: a dominant role for temperature . In: M.H. Nitecki (ed . ) Extinctions, pp. 69- 1 17. University of Chicago Press, Chicago. Stanley, S.M. 1987. Extinction . Scientific American Books, New York. Wilde, P. & Berry, W.B.N. 1984. Destabilisation of the oceanic density structure and its significance to marine extinction events . Palaeogeography, Palaeoclimatology, Palaeoecology 48, 143 - 162. Wolfe, J.A. & Upchurch, C . R . 1987. North American non-marine climates and vegetation during the late Cretaceous . Palaeogeography, Palaeoclimatology, Palaeo­ ecology 61, 33- 78 .

2 . 12.2 Extra-terrestrial Causes D . JABL O N SKI

Introduction Extra-terrestrial causes have long been invoked for mass extinctions, but only in the past decade has the general scientific community taken the idea seriously . Geochemical, sedimentary, and other signals in the stratigraphic record are sufficient to suggest that it is impossible to ignore extra­ terrestrial impacts as potential explanations for the biotic crises that punctuate the fossil record . The case is not fully proven for any single mass extinc­ tion, although it is strongest for the end-Cretaceous event (W. Alvarez 1986; L . W . Alvarez 1987; see Hallam 1987 and Officer et al . 1987 for different views; see also Sections 2 . 12 . 1 , 2 . 1 3 . 6, 2 . 1 3 . 7) . In any event, the initial discovery of iridium and other geochemical anomalies at the Cretaceous- Tertiary boundary has sparked an immense amount of inter­ disciplinary research on the problem of mass ex­ tinctions and potential extra-terrestrial forcing agents .

Potential mechanisms Proposed extra-terrestrial causes for mass extinc­ tions have included variation in solar heat output, massive solar flares, sudden influx of cosmic rays owing to a nearby supernova or the Solar System's crossing of the Galactic plane, and collisions with comets, asteroids, or other extra-terrestrial objects

2 . 1 2 Mass Extinction : Processes (collectively termed bolides) . Until recently such factors were at best subject to only the weakest verification based on approximate correlations in timing, and at worst simply reflections of desper­ ation in the face of seemingly inexplicable biotic upheavals . New lines of evidence for possible bolide impacts at one, and perhaps as many as five, extinc­ tion events have shifted these speculations into the realm of testability . Earth-crossing asteroids (asteroids whose orbits cross that of the Earth or could cross as a result of long-range gravitational perturbations) are suf­ ficiently common that significant bolide impacts must have occurred in the geological past. The Earth should suffer impacts by c. six 1 km asteroids per million years, and by c. two asteroids of 10 km ' or more per 100 million years, i . e . about a dozen large impacts since the beginning of the Phanerozoic (Shoemaker 1984) . Effects of 1 km objects are uncer­ tain but, as discussed below, most workers believe that impact by a 10 km bolide would have severe, global consequences . The average collision rate for comets is almost certainly lower than that for asteroids . Cometary impact rates could occasionally be raised, however, by perturbing the Oort cloud of comets that surrounds the Solar System far beyond the outer­ most planets (inner edge about 104 Astronomical Units (AU) from the Sun, where 1 AU is the distance from the Sun to the Earth) . Passage through the higher stellar densities in the spiral arms of the Galaxy might raise collision rates by about 10% (Shoemaker 1984) . This low-frequency modulation of cometary impacts would be punctuated ap­ proximately once per 100 million years by short­ lived bursts (1 - 3 million years) triggered by close passage of individual stars (Hut et al. 1987) . Evidence for periodic extinctions, still hotly de­ bated, suggests (but does not prove) a more regular and frequent perturbation of the Oort cloud . Hy­ pothesized mechanisms include : oscillations around the Galactic plane, where encounters with stars and molecular clouds would be most probable; a tenth planet in a highly eccentric orbit beyond Pluto (at c. 100 AU); and a dim solar companion star, christened Nemesis in advance of discovery (at distances variously estimated in the order of 104 - 105 AU) . Debates on the astronomical plausibility of these mechanisms, with Nemesis maintaining a slight edge, are reviewed by Shoemaker & Wolfe (1986) and Hut et al. (1987) (see also Section 2 . 1 2 . 3) . The magnitude and geographical scale of an im­ pact's effects depend on bolide size and velocity but

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thresholds have not been determined . An asteroid 10 km in diameter was estimated for the end­ Cretaceous event on the basis of global iridium levels, and although potential effects are still poorly understood they would probably have been severe . W. Alvarez (1986), L . W . Alvarez (1987) and Prinn & Fegley (1987) emphasize the following possibilities : 1 Darkness caused by the global cloud of fine dust particles generated by the impact. For 2 - 1 1 months, this darkness may have been sufficiently profound to halt photosynthesis, thereby causing the collapse of marine and terrestrial food chains. 2 Cold would accompany the darkness, with tem­ peratures dropping below freezing in continental interiors . Maritime climates would be less severely perturbed, owing to the thermal inertia of oceanic waters . 3 Greenhouse effects and global warming could fol­ low the cold-temperature excursion if the bolide(s) struck in the ocean . After dust grains coagulated and settled from the atmosphere, the remaining burden of water vapour could trap infrared energy reflected from the Earth and raise global tempera­ tures by as much as 100e . The duration of this greenhouse episode is uncertain, with estimates ranging from months or years to much longer spans than the immediate cold, dark aftermath - perhaps as long as 1000 years (Prinn & Fegley 1987) . 4 Nitric acid rain might result from shock heating of the Earth's atmosphere during impact (see Prinn & Fegley 1987, whose calculations are followed here) . Energy from atmospheric entry and, especially, the supersonic plume ejected upon impact would pro­ duce very large amounts of nitric oxides . These compounds would undergo a series of reactions and ultimately rain out as nitric and nitrous acid . On land this would severely damage foliage (and, presumably, animals) both directly and through mobilization of trace metals . In the ocean, within a decade or less, the acid rain could lower the pH of the mixed layer (especially the upper 30 m) to 7 . 5 - 7.8, sufficient to dissolve calcite and thus severely stress calcareous organisms . Further, in­ jection of so much strong acid into the atmosphere would elicit a significant exhalation of oceanic CO 2, which, combined with the accumulation of CO2 in the atmosphere owing to depressed activity of marine phytoplankton, would yield greenhouse warming over thousands of years . This impressive menu of impact-driven pertur­ bations could be expected to cause mass extinc­ tions of the observed magnitudes . Indeed, a

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number of palaeontologists have argued that the hypothesized perturbations are too severe for the observed extinctions, even at the Cretaceous ­ Tertiary boundary (e . g . Hallam 1987) . However, the impact-effect models are very poorly constrained and require extrapolation far beyond hard obser­ vational data; a new generation of more realistic and sophisticated models may provide an improved basis for critically comparing hypothesized causes with observed extinction patterns .

Biological evidence The initial impetus for seeking extra-terrestrial im­ pacts was of course the biological pattern of extinc­ tion in the fossil record, whether perceived as peaks in global extinction rates or as disap pearances of taxa or biomass in local sections . Unfortunately, the biological consequences of impacts, massive vol­ canism, and other alternatives are not sufficiently understood or sufficiently unique to provide critical tests . Complex biological upheavals enacted on scales of months, years or decades, as postulated by impact scenarios, are extremely difficult, often im­ possible, to resolve in single stratigraphic sections, and challenge the limits of global correlation . Short­ term events are superimposed on more protracted patterns in the expansion and contraction of taxa, owing to Earth-bound physical and biotic factors, so that the effect of a given boundary event on a particular taxon (particularly a waning one) is de­ batable . At present, the strongest constraints that palaeontological data can provide involve consist­ ency between a given mechanism and the biological pattern observed in an imperfect fossil record .

Onset and aftermath. For extra-terrestrial impacts, biological responses include abrupt onset of extinc­ tion with an extremely brief crisis period, and a re­ latively short-lived reorganization and rebound during return to pre-impact conditions . In end­ Cretaceous impact models, for example, most en­ vironmental perturbations would last only 1 - 10 years, an interval impossible to correlate among distant localities, and within which events are vir­ tually unresolvable in the geological record . Geo­ logically abrupt onset of mass extinction is a requirement but not a unique prediction of impact hypotheses : even such gradual processes as marine regression or transgression could in principle carry threshold effects that would produce sudden ex­ tinction pulses on stratigraphically-resolvable time­ scales.

Hypothesized greenhouse warming, and possibly other palaeoceanographic anomalies, would persist for some thousands of years beyond the impact itself. Some palaeontological (and geochemical) evidence supports a geologically brief - but eco­ logically protracted - recovery period, particularly in terrestrial plants (reviewed by Wolfe 1987) and marine plankton (reviewed by Zachos & Arthur 1986), although, again, these would not be unique to extra-terrestrial events . Extinction patterns observed at critical bound­ aries cannot be taken at face value . Seemingly abrupt extinction can result from erosion or non­ deposition of sediments during the critical time interval, so that biological events are compressed into single beds . At the same time, artificially gradational extinction patterns result when sam­ pling deteriorates, or is simply uneven, in the in­ terval approaching the boundary (a phenomenon termed backwards-smearing, or the Signor- Lipps effect - see Jablonski 1986a; Raup 1987) . Step wise patterns of extinction, with pulses of extinction arrayed around a mass extinction boundary, have been claimed to reconcile the re­ quirements of abrupt extinction with observations that seemed to suggest gradual loss of taxa . Such stepwise patterns - with up to 12 discrete extinc­ tion events claimed near the Cretaceous- Tertiary boundary - are also taken as the geologically rapid succession of extinction events expected during cometary bombardment . These stepwise patterns are distinct from prolonged patterns of decline such as suggested for Late Cretaceous ammonites, and are recorded near the Cenomanian - Turonian, Cretaceous- Tertiary, and Eocene - Oligocene boundaries (Hut et al. 1987) . Unfortunately, such patterns cannot yet be taken at face value, because they can also be generated by sampling effects, local ecological changes, and/or minor breaks in sedi­ mentation imposed on either abrupt or gradational extinction . Lazarus taxa (which seem to suffer extinction but then reappear later in the stratigraphic record; Jablonski 1986a; Raup 1987) provide one means of partially controlling for unevenness in sampling and preservation : the proportion of Lazarus taxa, i . e . of observed last appearances that represent artificial extinction, permits a rough quantitative assessment of the reliability of extinction data with­ in and around critical time intervals . Most stepwise extinction sequences contain some Lazarus taxa, suggesting that sampling effects are indeed a factor. More rigorous and comprehensive approaches are

2 . 1 2 Mass Extinction : Processes required to place confidence limits on bed-by-bed extinction patterns . Detailed studies of critical time intervals are urgently needed, but the plea for more centimetre by centimetre sampling near extinction events is somewhat misguided. At that scale, local ecological effects, the vagaries of sampling, and even biotur­ bation are likely to overwhelm the fine structure of global events . Careful sampling of relatively long geological sequences that encompass extinction events would be especially valuable, so that absences as well as presences could be recorded throughout, to provide some statistical control . Consistency of extinction patterns among widely separated localities also should be sought in a criti­ cal fashion; caution is necessary, particularly for apparent stepwise patterns, because different taxa - say, ammonites and benthic gastropods have different sampling characteristics, even on broad geographical and temporal scales (see Jablonski 1986a on the biology of Lazarus taxa) .

Selectivity has been claimed for most mass extinc­ tions : large-bodied taxa, reef-dwellers or tropical organisms in general, and endemic taxa all appear to suffer preferential extinction (Jablonski 1986a, b) . Critics (and some supporters!) of impact hypotheses have claimed that impact-driven extinction would be random rather than selective, so that any observed taxonomic or ecological selectivity would be contrary evidence . This claim seems inappro­ priate, however: taxa differ in their vulnerability to environmental change, so that any given pertur­ bation, regardless of scale, should affect some groups more severely than others . Survivorship of widespread taxa, non-tropical taxa, small-bodied taxa, members of detrital food chains, freshwater taxa, deciduous plants, and plankton whose life cycles include resting cysts, has been claimed for the end-Cretaceous extinction (Jablonski 1986a, b; Hallam 1987) . All are consistent with, but not ex­ clusive to, impact hypothese s . Similarly, the pos­ sibility that mass extinctions are qualitatively different from background extinctions in their vic­ tims (e .g. see Jablonski 1986a, b) does not require impact events - any perturbation of sufficient magnitude could, for example, cross a threshold of extinction effects so that broad geographical range could determine survivorship but species richness was no longer important. Periodicity. The apparent periodicity of post­ Palaeozoic extinction events has sparked much re-

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search and speculation on extra-terrestrial forcing factors (see also Section 2 . 12.3) . The periodicity it­ self, however, is not an adequate test for extra­ terrestrial causes, although few alternatives have been advanced (Hallam 1987 reviewed a hypothesis of endogenous periodicity in mantle plumes; see also Section 2 . 1 2 . 1 ) . Clearly, the critical role for palaeontological data in testing for extra-terrestrial causes of mass extinctions lies in the degree of correspondence between biological events and independent physico-chemical evidence for impacts or other extra-terrestrial forcing mechanisms . As discussed below, however, assembling such evi­ dence is not as straightforward as was once hoped.

Physical evidence Several physico-chemical phenomena have been proposed as independent evidence for extra­ terrestrial impact . Although each has its critics, and some may not be strictly diagnostic, taken together the data make a strong case for the end-Cretaceous and Late Eocene extinctions, with weaker but suggestive evidence for several other post­ Palaeozoic events (Raup 1987) . The strongest Earth­ bound alternative at this time appears to be volcanism (Hallam 1987; Officer et al. 1987; see also Section 2 . 12 . 1 ) .

Geochemical. The anomalously high concentrations in Cretaceous - Tertiary boundary sediments of iridium, and other elements scarce in the Earth's crust but abundant in asteroids, launched the Alvarez hypothesis that an end-Cretaceous impact caused the mass extinction . Since 1979 this anomaly has been found at over 75 localities world-wide (Fig . 1) in deep-sea, shallow-marine, and continen­ tal palaeoenvironments, usually in a distinctive clay layer that coincides (within stratigraphic uncer­ tainty limits) with the extinction event (W. Alvarez 1986; L . W . Alvarez 1987) . Excursions in oxygen and carbon isotopes near the boundary also suggest a low-productivity episode that may have lasted 1 . 0 million years or more, accompanied by detectable but unexceptional temperature oscillations (Zachos et al. 1989) . The direction of the stable isotopic fluctuations is appropriate to impact hypotheses, but the duration seems too long and the temperature changes too mild (but see above discussions on uncertainties in impact models and limits in stratigraphic resolution) . None of the other four major mass extinctions of the Phanerozoic has such strong geochemical

2 The Evolutionary Process and the Fossil Record

168

.. . . .

. . ...

.

•

Fig. 1

Global distribution of iridium anomalies in Cretaceous - Tertiary sediments . (After L.W. Alvarez 1987.)

anomalies known from so many localities, although far less effort has been devoted to the search (Jablonski 1986a; Donovan 1987a; Raup 1987) . Slight end-Ordovician iridium enrichments seem to be terrestrial in origin; the end-Triassic results are negative so far; the reported end-Permian anomaly, at the largest mass extinction of them all, has not been repeated by other laboratories, and the boundary clays seem volcanic in origin; the Late Devonian (Frasnian -Famennian) anomaly occurs in an unusual stromatolitic deposit and has not been replicated in other boundary sections . Among lesser extinction events, iridium anomalies are geographically widespread near the Eocene - Oligocene extinction boundary, along with a series of microtektite horizons whose impact origin is virtually uncontested (Hut et al. 1987) . An iridium anomaly was recently discovered (L . W. Alvarez 1987) for the small Middle Miocene extinction that forms the most recent peak in periodicity analyses, although the global extent of the iridium is as yet unknown . The Cenomanian - Turonian boundary has excess iridium, but other impact signatures are lacking and a terrestrial origin may be involved . An anomaly at the Middle - Upper Jurassic bound­ ary - where no extinction event occurs but is predicted by periodicity models - occurs (like the Frasnian - Famennian example) in stromatolitic sediments, raising the spectre of biological or dia-

genetic concentration . Age uncertainty of an iridium anomaly in a 2 - 3 mm iron-rich crust at an uncon­ formity in the Southern Alps overlaps with another weak or 'missing' (i . e . predicted by periodicity models) extinction peak in the Bajocian (Rocchia et al. 1986) . An iridium anomaly, with other cosmic debris, is recorded from Late Pliocene sediments in the Southern Ocean, coinciding in time but not in space with a regional extinction event in the North Atlantic . The situation is further complicated by an anomaly near the base of the Cambrian, at a level lacking mass extinction and well after the beginning of the Cambrian radiation of skeletonized organisms (Donovan 1987b) . The degree to which all of these iridium anomalies denote impacts is still debated (Hallam 1987; Officer et al. 1987; Section 2 . 12 . 1 ) . Iridium enrichments may extend for metres around the Cretaceous ­ Tertiary boundary in some key sections; the signifi­ cance of these new observations is unclear, with interpretations ranging from diagenetic mobili­ zation from an impact-fallout layer to prolonged deposition from volcanic aerosols . An aerosol from the Hawaiian volcano Kilauea was highly enriched in iridium, apparently derived from the deep mantle; however, other elements in the aerosol do not mimic the extra-terrestrial abundances in end­ Cretaceous boundary sequences (W. Alvarez 1986) so that, again, the significance of these data is uncer-

2 . 1 2 Mass Extinction : Processes

169

tain. Boundary clay compositions do not always correspond to extra-terrestrial elemental abun­ dances and isotope ratios, and yield conflicting evi­ dence regarding the nature of the hypothesized bolide . It is not clear whether post-impact diagenetic overprint or multiple impacts by bolides of different compositions (expected in cometary bombard­ ment?) can account for such inconsistencies . New analytical techniques (1 . W. Alvarez 1987) will per­ mit much more extensive stratigraphic coverage, both at extinction boundaries and at quiet times in between, and thus greatly improve understanding of the global iridium flux and potential nonextra­ terrestrial enrichment mechanisms . Fig.

Mineralogical. Potential independent ' evidence for impact comes from shock-metamorphosed quartz and other sedimentary particles . Like iridium, quartz grains with at least two and up to nine intersecting sets of shock lamellae have been found in Cretaceous- Tertiary boundary sequences throughout the world, in both marine and conti­ nental settings (Fig. 2) (Bohor et al . 1987a; Izett 1987) . Such multiple lamellae are known only in particles from nuclear testing sites and impact craters . Shock-metamorphosed minerals do form near certain explosive volcanic eruptions (Hallam 1987), but the multiple lamellae and the world-wide distribution of the relatively large grains (0 . 1 0 . 2 mm in North Pacific and New Zealand sedi­ ments, up to 0 . 6 mm in North America) are difficult to reconcile with volcanic activity (W . Alvarez 1986; Bohor et al. 1987a) . The search for shock­ metamorphosed minerals at other extinction events has been negative so far, except for an intriguing preliminary report near the Triassic -Jurassic boundary in Austria (Badjukov et al. 1987) .

Sedimentological. Microtektites (glassy droplets formed by bolide impacts) are almost undoubtedly present at three horizons near the Eocene ­ Oligocene boundary (Hut et al. 1987) . A similar origin has been suggested for spherules of dis­ ordered potassium-feldspar (sanidine), glauconite, goethite, and magnetite found world-wide in Cretaceous -Tertiary sequences (W . Alvarez 1986), but recent evidence suggests an authigenic, non­ impact origin for at least some spherules (Hallam 1987; Izett 1987) . Microspherules of varying com­ position occur in Permo-Triassic boundary sedi­ ments in Sichuan, China (Gao et al. 1987); their significance is uncertain in the light of the seemingly volcanic origin of the boundary clays in China.

2 Shocked quartz grain from Cretaceous -Tertiary boundary clay in a non-marine section at Brownie Butte, Garfield County, Montana. Scanning electron micrograph, width of field 0 . 14 mm. (Courtesy of B.F. Bohor.)

More work is needed in separating spherules of different origins before interpretations are possible (Bohor et al. 1987b) . Soot particles are abundant in Danish and New Zealand Cretaceous - Tertiary boundary clays (W . Alvarez 1986; 1 . W . Alvarez 1987) . If these clays rep­ resent only one year of deposition, as postulated by most impact models, the carbon flux would have been 10 3 - 104 above background levels, suggesting extensive wildfires triggered by the heat of impact or propagated among the remains of forests killed by the hypothesized post-impact cold interval . How­ ever, the uniqueness of such soot occurrences is uncertain, and the high flux depends on the duration of clay layer deposition, which is still debated (Hallam 1987) .

Cratering. Major impacts should leave craters at least an order of magnitude larger than the bolide itself. Age uncertainties are troublesome and the data are extremely sparse, but the association be­ tween extinction events over the past 250 million years and the 26 well dated craters of 5 km or more in diameter may be statistically significant (re­ viewed by Shoemaker and Wolfe 1986, who are sceptical) . Simulations by Trefil & Raup (1987) suggest that this cratering record comprises about one-third periodic impacts (presumably comet showers) and two-thirds random collisions with asteroids . Shoemaker & Wolfe (1986) reach a similar conclusion by different means . Questions emerge about the best-studied extinc­ tion event, however . The only well dated craters of appropriate size near the Cretaceous- Tertiary

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boundary are in the U . S . S .R. (Shoemaker & Wolfe 1986), but the size and density of shocked quartz grains suggests an impact in North America (Bohor et al. 1987a; Izett 1987) . Further, the shocked quartz suggests an impact in sedimentary rocks, i . e . a con­ tinental or shallow-water setting, whereas mag­ netite and other spherules suggest altered basalt, and thus an oceanic impact (although impact deri­ vation of the spherules is now questioned, as noted above) . These contradictions are perhaps resolvable with an end-Cretaceous comet shower and the consequent multiple impact, but the problem of impact site(s) remains (Hallam 1987) . A volcanic interpretation is no more satisfactory in this regard .

Conclusion and prospects Although no one indicator is definitive, at present the diverse physical and chemical evidence at the Cretaceous -Tertiary boundary is most readily ex­ plained by a bolide impact . Volcanism is the chief rival, but as W. Alvarez (1986) argued, evidently only quiet basaltic eruptions yield iridium aerosols and melt microspherules, whereas violent siliceous eruptions are needed to produce shocked minerals . Neither kind of eruption will produce all of the observed impact signatures, nor can either account for the world-wide distribution of shocked quartz, iridium and other geochemical anomalies . The periodic mantle plume hypothesis might yield both explosive and non-explosive volcanism on a global scale (Hallam 1987; Section 2 . 12 . 1), but this model awaits evaluation . The palaeontological data are generally consistent with, but provide little con­ clusive support for, impact-driven extinction mech­ anisms . As many authors have noted, marine re­ gression at this and other extinction events obscures biological and physico-chemical signals and may even play a role in extinction (Section 2 . 12 . 1 ) . The most definitive evidence for or against extra­ terrestrial factors in mass extinctions (apart from the discovery of the hypothesized solar companion, Nemesis) will come with an assessment of the strength of temporal association between Phanero­ zoic mass extinctions and physico-chemical signa­ tures of bolide impacts . This work is under way, and it is impressive that the three or four most recent extinction peaks recognized in global data sets and/or local strati graphic sections (Middle Miocene, Eocene - Oligocene, Cretaceous- Tertiary, and Cenomanian - Turonian) bear at least some impact indicators . The weak but significant cluster­ ing of crater ages at extinction events over the past

250 million years should prompt analyses around other boundaries, with ongoing refinement of hypotheses . Assessment of negative evidence re­ mains a problem, however, so that impact hypoth­ eses can be remarkably elastic and difficult to falsify : absence of craters, shocked quartz and even iridium anomalies are consistent with impact on now­ subducted ocean, basaltic impact site, and cometary rather than meteorite impact, respectively. Addition­ ally, not all major craters, microtektite horizons, or iridium anomalies coincide with extinction events . Better understanding of the potential effects of im­ pacts, and of the distribution of potential impact signatures through the stratigraphic record, should lead to the framing of more refined hypotheses regarding the role of extra-terrestrial factors in the evolution of life on Earth .

References Alvarez, L.W. 1987. Mass extinctions caused by large bolide impacts . Physics Today 40, 24 -33. Alvarez, W., 1986 . Toward a theory of impact crises . Eos 67, 649, 653 -655, 658. Badjukov, D . D . , Lobitzer, H. & Nazarov, M.A. 1987. Quartz grains with planar features in the Triassic-Jurassic boundary sediments from Northern Limestone Alps, Austria. Lunar and Planetary Science 18 , 38 -39. Bohor, B . F . , Modreski, P.]. & Foord, E.E. 1987a . Shocked quartz in the Cretaceous -Tertiary boundary clays: evidence for a global distribution. Science 236, 705 - 709 (see also 666 - 668) . Bohor, B . F . , Triplehorn, D . M . , Nichols, D.J. & Millard, H.T., ]r. 1987b. Dinosaurs, spherules, and the 'magic' layer: a new K-T boundary clay site in Wyoming. Geology 15, 896 - 899 . Donovan, S.K. 1987a. Iridium anomalous no longer? Nature 326, 331 -332 . Donovan, S.K. 1987b . Confusion at the boundary. Nature 329, 288 . Gao Zhengang, Xu Daoyi, Zhang Qinwen & Sun Yiyin 1987. Discovery and study of microspherules at the Permian­ Triassic boundary of the Shangsi section, Guangyuan, Sichuan. Geological Review 33, 203-211 (in Chinese with English abstract) . Hallam, A. 1987. End-Cretaceous mass extinction event: argument for terrestrial causation . Science 238, 1237-1242. Hut, P., Alvarez, W., Elder, W . P . , Hansen, T., Kauffman, E . G . , Keller, G . , Shoemaker, E . M . & Weissman, P.R. 1987. Comet showers as a cause of mass extinctions. Nature 329, 118- 126. Izett, G.A. 1987. Authigenic 'spherules' in K-T boundary sediments at Caravaca, Spain and Raton Basin, Colorado and New Mexico, may not be impact derived . Bulletin of the Geological Society of America 99, 78- 86. ]ablonski, D. 1986a . Causes and consequences of mass extinctions : a comparative approach . In: D.K. Elliott (ed . )

2 . 1 2 Mass Extinction: Processes Dynamics of extinction, pp . 183-229 . Wiley, New York. Jablonski, D. 1986b . Evolutionary consequences of mass extinctions . In: D.M. Raup and D. Jablonski (eds) Patterns and processes in the history of life, pp . 313-329 . Springer­ Verlag, Berlin . Officer, C B . , Hallam, A . , Drake, C L . & Devine, J . D . 1987. Late Cretaceous and paroxysmal Cretaceousrrertiary extinctions . Nature 326, 143 - 149 . Prinn, R.G. & Fegley, B . , Jr. 1987. Bolide impacts, acid rain, and biospheric traumas at the Cretaceous-Tertiary boundary. Earth and Planetary Science Letters 83, 1 - 15 . Raup, D.M. 1987. Mass extinction: a commentary. Palaeon­ tology 30, 1 - 13 . Rocchia, R., Boclet, D . , Bonte, P . , Castellarin, A. & Jehanno, C 1986 . An iridium anomaly in the Middle - Lower Jurassic of the Venetian region, northern Italy . Journal of Geophysical Research 91, E259 - E262. Shoemaker, E . M . 1984. Large body impacts through geologic time. In: H.D. Holland & A.F. Trendall (eds) Patterns of change in Earth evolution, pp. 15 -40. Springer-Verlag, Berlin. Shoemaker, E . M . & Wolfe, R. 1986 . Mass extinctions, crater ages, and comet showers. In: R.S. Smoluchowski, J.N. Bahcall & M . 5 . Matthews (eds) The galaxy and the solar system, pp. 338 -386. University of Arizona Press, Tucson. Trefil, J . 5 . & Raup, D.M. 1987. Numerical simulations and the problem of periodicity in the cratering record. Earth and Planetary Science Letters 82, 159 - 1 64. Wolfe, J.A. 1987. Late Cretaceous- Cenozoic history of de­ ciduousness and the terminal Cretaceous event. Paleo­ biology 13, 215-226. Zachos, rC & Arthur, M.A. 1986. Paleoceanography of the Cretaceousrrertiary boundary event: inferences from stable isotopic and other data. Paleoceanography 1, 5-26. Zachos, J.C, Arthur, M.A. & Dean, W.E. 1989 . Geochemical evidence for suppression of pelagic productivity at the Cretaceous/Tertiary boundary . Nature 337, 61 -64.

2 . 12 . 3 Periodicity J . J . S E P K O S KI , Jr

Introduction Periodicity of extinction is a hypothesis that ex­ tinction events (both mass extinctions and their less severe analogues) have occurred at regularly spaced intervals through geological time . It is an empirical claim based upon statistical analyses of the fossil record which indicate that maxima in extinction intensity, recognized in both biostratigraphic studies and taxonomic data compilations, are de­ cidedly non-random with respect to time and seem to fit a regular, periodic time series. This hypothesis was introduced by Fischer & Arthur (1977) for

171

patterns of diversity in open-ocean pelagic com­ munities and later supported by Raup & Sepkoski (1984), who claimed a 26 million year periodicity in extinction of global marine families . The hypothesis has since proved very controversial largely as a result of association with suggestions of catas­ trophic, extra-terrestrial forcing agents .

Meaning of periodicity A perfectly periodic time series has regularly spaced events separated by invariant waiting times (Fig. 1 ) . I n most o f the debate about periodicity, this pattern has been contrasted with a 'random', or Poisson, time series . A Poisson series can arise when events are independent of one another and determined by a large number of unrelated factors . A classic example is coin flipping, in which the outcome (heads or tails) of each trial results from a multitude of in­ dependent forces . The lower time series in Fig. 1 was generated by flipping a pair of coins and re­ cording when both came up heads . The frequency of events (one in four trials) is the same as in the upper, periodic series, but the appearance is very different . The lower series is composed of loose clusters of events with irregular gaps in between; waiting times approach an exponential distribution with the median waiting time shorter than the average frequency . The relevance of these considerations to the study of extinction events is that traditionally each event has been analysed in isolation from others and independent causal hypotheses have been formu­ lated . Implicit in this is the assumption that extinc­ tion events must be randomly spaced in time . Observation of regular spacing, however, implies some organizing principle to extinction events, either some set of factors that governs waiting times so that they appear invariant, or some single ulti­ mate forcing agent that has clock-like properties . Periodicity can also imply that the proximate agent of any one extinction event is the same for all, although this is not a necessary implication if the chain of causation is complex. The association of periodicity with catas trophism comes from these last considerations . In particu­ lar, it has been suggested that: (1) the claimed 26 million year periodicity of extinction events is too long to have been produced by any known terres­ trial process with periodic behaviour, leaving some astronomical clock as the likely forcing agent; and (2) the association of the Cretaceous - Tertiary mass extinction with evidence of a large extra-terrestrial

2 The Evolutionary Process and the Fossil Record

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impact (Section 2 . 12.2) suggests (as a hypothesis to be tested) that other events in the periodic series might have been similarly caused . Note that these arguments suggest only a possible association, and other, terrestrial mechanisms are still conceivable (Section 2 . 12 . 1 ) .

Evidence for periodicity The hypotheses of periodicity put forward by Fischer & Arthur (1977) and Raup & Sepkoski (1984) were based upon compilations of diversity data and ex­ tinction times for taxa in the marine fossil record . Fischer & Arthur were concerned with recurrent fluctuations in the diversity of globigerinid species, ammonoid genera, and large pelagic predators through the Mesozoic and Cenozoic . They argued, without rigorous statistical testing, that these fluc­ tuations were cyclic with a 32 million year waiting time . Using family-level data for the entire marine ecosystem, updated time-scales, and a variety of statistical tests, Raup & Sepkoski corroborated the Fischer -Arthur hypothesis but concluded that the period length was closer to 26 million years . Their statistical tests (which included parametric Fourier and autocorrelation analyses and non-parametric randomization analysis) all indicated a significant non-randomness in the distribution of extinction events and a good, but not perfect, fit to a periodic series. Raup & Sepkoski's (1984) treatment and testing of familial extinctions were somewhat complex and have led to some confusion . Their analysis was limited to families in the Late Permian through Neogene, where stratigraphic stages are shorter and more accurately dated than in the preceding Palaeozoic. To enhance resolution, only families with extinctions known to the stage level were used

and taxa of soft-bodied and lightly sclerotized ani­ mals, or of very uncertain taxonomic position, were rejected . These manipulations left a data set of 567 extinct families ranging over 39 stratigraphic stages. Extinction intensity was measured by percent ex­ tinction, the number of extinctions in a stage div­ ided by diversity . This metric (statistical measure) scales extinction to the number of families at risk in any stage but does not incorporate estimates of stage duration, which have limited accuracy . Percent extinction for families exhibits very low values over the Cenozoic, leaving peaks of extinction difficult to discern; Raup & Sepkoski therefore used only the diversity of families extinct before the Recent in the denominator of the metric, inflating its values in the Cenozoic . The time series constructed by this treatment (Fig. 2) contains 'peaks', or local maxima, that vary considerably in height. Raup & Sepkoski recognized that some of these (e . g . the Guadalupian, Rhaetian, and Maastrichtian) correspond to well documented mass extinctions, but that some of the lower peaks might be spurious . Nevertheless, they chose to ana­ lyse all peaks rather than a selected subset, in order to avoid possible subjective bias . Unfortunately, they referred to all 12 peaks as 'mass extinctions' . A randomization test for periodicity was favoured by Raup & Sepkoski (1984) because it permitted fitting a wide band of period lengths and was not sensitive to unequal spacing of data (imposed by the stratigraphic time-scale) or to variation in mag­ nitudes of extinction peaks (which were presumed to fluctuate freely) . The test (which is akin to boot­ strap procedures) involved fitting periodicities to the observed extinction peaks and then comparing the goodness of fits to randomized (i . e . shuffled) versions of the data . The peaks were treated as if they all fell at the ends of stages; this, however, was merely a formalization, and equivalent results would have obtained if the peaks were consistently placed at the middles or beginnings . The shuffling procedure converted the data into what was essen­ tially a random walk with the only constraint being that peaks must be separated by at least two stages. The randomization test showed that periodicity fits the observed data better than 99 . 99% of random walks at 26 million years, even though the fit to the peaks (especially the smaller peaks) was not perfect (Fig . 2) . On this basis, Raup & Sepkoski concluded that there was a 26 million year periodicity to 'mass extinctions' through the Mesozoic and Cenozoic Eras . No periodicity was found in the Palaeozoic, however. Rampino & Stothers (1984) corroborated

2 . 1 2 Mass Extinction: Processes

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this result, even after eliminating the three smallest peaks in the time series . A similar period-fitting technique applied to the nine remaining peaks gave a 26 million year period . However, a regression­ based technique resulted in a 30 million year period, which they favoured on other grounds . Subsequent analyses performed by Raup & Sepkoski were designed to counter criticisms of their data manipulation and statistical procedures, and to explore the correspondence between global taxonomic data and information from biostrati­ graphic studies . Sepkoski & Raup (1986) re analysed the familial data using all extinctions (other than those of soft-bodied animals tied to Konservat ­ Lagerstatten; Section 3 . 1 1 ) and employing total di­ versity in the metrics . Fig . 3 illustrates the time

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series for percent extinction in this analysis . Three other metrics of extinction were also computed and an attempt was made to assess which extinction peaks could be considered statistically significant . Sepkoski & Raup determined only eight o f their previous 12 peaks to be significant and found that the heights of these peaks were generally lower than in the highly culled data set . They argued, however, that seven of the peaks corresponded to extinction events recognized by palaeontologists working at the species level with material collected from outcrops and cores . This indicated to the authors that global familial data could be trusted to reflect important extinction patterns among species in the fossil record . Sepkoski & Raup (1986) found that the random-

2 The Evolutionary Process and the Fossil Record

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ization test applied to the eight extinction peaks still indicated a significant periodicity at 26 million years, with the standard error judged to be about ± 1 million years when imprecisions in the time­ scale were accommodated . In a companion paper, Raup & Sepkoski (1986) showed that the level of statistical significance of the randomization test varied somewhat if different ages were assigned to the less precisely dated events (end-Permian and end-Triassic) . Still, they concluded that most fits of the 26 million year periodicity were significant at or above the 95% level, even after adjustment for the problem of multiple tests (i . e . testing many fre­ quencies in the 1 2 - 60 million year band) . Raup & Sepkoski (1986) and Sepkoski (1986) also conducted analyses at the generic level, using a new compilation for global marine animals . This was done to increase sample size and to obtain a better approximation of species patterns . Higher taxa tend to damp the signal of species extinction since all species within a polytypic taxon must disappear for the taxon to register an extinction event . The new data set contained nearly 10 000 genera in the inter­ val from Upper Permian to Recent . It also incorpor­ ated a refined stratigraphic time-scale with 51 intervals (in contrast to the previous 39 -43 stages) . Fig . 4 illustrates one of four time series for generic extinction . As expected, the eight peaks of extinction

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are more prominent than in the familial data . The peak in the Middle Miocene seems to be confirmed and an extinction event is suggested in the Aptian, which previously appeared as a gap in the periodic sequence (Fig . 3) . A gap still exists in the Middle Jurassic despite two questionable peaks (Lower Bajocian and Oxfordian) . These two peaks, as well as the Carnian peak (to the left of the Upper Norian peak in Fig . 4), fluctuate erratically with different metrics of extinction, suggesting that they are not robust features of the data . Raup & Sepkoski (1986) performed the random­ ization test on these data and concluded that they contained the 26 million year periodicity of extinc­ tion . Sepkoski (1986) also performed autocorrelation analyses (i . e . correlating a time series with itself at a given time lag, which assesses amplitude as well as wavelength) and obtained statistically significant results consistent with a 26 million year periodicity . Finally, Fox (1987) performed an elaborate series of Fourier analyses on the generic data and also found a significant 26 million year periodicity . This was true even when he split the time series into two parts: both halves displayed a periodicity with the same wavelength and, very importantly, nearly the same phase . None of these analyses of the generic data showed decisive evidence for a periodicity prior to the Permian, however, although Sepkoski

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2 . 1 2 Mass Extinction: Processes I

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Critiques of periodicity The hypothesis of periodicity in extinction engen­ dered immediate attention from scientists as well as the popular press . Not surprisingly, this led to intense scrutiny of both the data and the statistical analyses . The result has been a complex series of critical discussions with various responses by Raup & Sepkoski (see Sepkoski 1989), which can only be briefly summarized here .

Data. The validity of compilations of taxonomic data has been questioned by several authors . Hoffman (1985) argued that familial data are very noisy and that different treatments, including ap­ plication of alternative time-scales, results in dif­ ferent, seemingly random patterns of extinction peaks . This claim was countered by Sepkoski & Raup's (1986) demonstration of consistency of eight extinction peaks under four different metrics and by Sepkoski' s (1986) argument that even Hoffman's composite data display strong periodicity . The pres­ ence of the same periodic extinction peaks in the much larger generic data would also seem to indi­ cate signal rather than noise . Stigler & Wagner (1987), however, argued that periodicity even in the generic data could be an artifact of imperfect sampling of the fossil record . Failure to sample taxa in their last stage of existence will smear the record of extinction backward in time . This will tend to swamp some minor extinction

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peaks between major maxima and cause the time series to appear more regular than expected for a Poisson distribution . The counterargument to this claim (Sepkoski & Raup 1986) is simply that detailed biostratigraphic investigations corroborate most of the extinction peaks evident in the generic data, and do not indicate many smaller extinction events in other stages (although some major extinction events may be composites of tightly clustered steps) . Patterson & Smith (1987) questioned the accuracy of any taxonomic compilation that contains para­ phyletic taxa (see Section 5 . 3) . They claimed that three-quarters of the families of echinoderms and vertebrates used by Raup & Sepkoski were para­ phyletic, monotypic, and/or misdated. When a cor­ rected monophyletic component (equivalent to 10% of Raup & Sepkoski's total data set) was examined, no periodicity was evident . Sepkoski (1987) re­ sponded that paraphyly in itself should not be a problem since family extinctions simply represent a sample of species extinctions . He further noted that the monophyletic taxa in Patterson & Smith's analysis failed to show some well documented extinction events (e . g . the Maastrichtian mass extinction) and suggested that this might be due to small sample size, idiosyncracies in the echinoderm and ver­ tebrate records, or biases inherent in the cladistic culling. Inaccuracies in the estimated ages of stratigraphic intervals used in the data sets pose numerous prob­ lems . As noted above, Hoffman (1985) argued that use of different time-scales causes differences in extinction peaks . Shoemaker & Wolfe (in Smoluchowski et al. 1986) assessed the estimated

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ages of Raup & Sepkoski's (1984) 12 extinction peaks and concluded that only three (the Cenomanian, Maastrichtian, and Upper Eocene) were reliable; this was too small a sample to support periodicity . Raup & Sepkoski (1986), however, showed that their randomization test did give significant results for the last four, best-dated extinction events (including the Middle Miocene event which Shoemaker & Wolfe rejected on the basis of familial data, but which Raup and Sepkoski accepted on the evidence of the generic data) . Stigler & Wagner (1987) questioned the strength of this test, arguing that the 26 million year period­ icity might be embedded in the time-scale . This is not surprising, however, since some stratigraphic boundaries are placed at points of major turnover (e . g . the Palaeozoic - Mesozoic and Mesozoic ­ Cenozoic boundaries) . Potential coupling of the stratigraphical and biological records was recog­ nized by Raup & Sepkoski (1984, 1986), who shuffled the time-scale in their tests in order to avoid this problem . It should be noted that the 51-interval time-scale used in the generic data, with longer stages subdivided and shorter stages amalgamated, does not display any embedded 26 million year periodicity .

Statistical analyses. Many technical aspects of the statistical tests conducted by Raup & Sepkoski have been questioned. Hoffman & Ghiold (1985) claimed that the analyses did not properly test for a random walk . They argued that the familial data displayed a mean frequency of one peak in every four stages, which is indistinguishable from the expectation of a random walk. But these authors (and likewise Noma & Glass 1987) failed to recognize that Raup & Sepkoski' s randomization procedure in essence converted the extinction data into random walks (although perhaps with less variance than proper, as pointed out by Quinn (1987» . Also, Sepkoski's (1986) auto correlation analysis with the refined time-scale showed a peak every fifth interval in the generic data, which is not consistent with a random walk . Noma & Glass (1987) used turning points in the familial data to argue that the hypothesis of ran­ domness could not be rejected. However, their test was very sensitive to variance in stage durations (which range from 1 million years for the Coniacian to 1 5 . 5 million years for the Albian), and it is unclear whether Noma & Glass demonstrated anything more than this variance . They also argued that there were flaws in the selection of 'significant' extinction

peaks by Raup & Sepkoski (1986) (as well as Sepkoski & Raup 1986) . This argument is valid, and at best Sepkoski & Raup merely eliminated demon­ strably insignificant peaks from their familial analyses. However, other evidence presented by Sepkoski & Raup suggests that the remaining eight peaks were not insignificant since : (1) the same peaks appeared even more prominently in the gen­ eric time series (Fig. 4); and (2) most of the peaks correspond to independently identified events in biostratigraphic analyses . Kitchell & Pena (1984) re analysed the familial data assuming equal durations of stages and apply­ ing a series of autoregressive models (i . e . regression equations in which values in each time interval are predicted from values in preceding intervals) . They rejected a simple model with periodic impulses but found adequate fits with a model incorporating five-stage memory, which they concluded dem­ onstrated only pseudoperiodicity in the data. How­ ever, the rejected simple periodic model imposed a regular amplitude as well as wavelength, and re­ quired equal numbers of stages between extinction peaks . (The number of stages between Raup & Sepkoski's periodic peaks varied from two to six; see Fig . 2) . Again, Sepkoski's (1986) autocorrelation analysis of the generic data suggested that a simple periodic impulse model could provide a statistically significant fit when the stratigraphic intervals were adjusted to be more equal in length . Quinn (1987) criticized Raup & Sepkoski's (1984) randomization test for ignoring the auto correlation in the data (although Stigler & Wagner (1987) did not consider this to be a problem) . Quinn failed to note that Raup and Sepkoski had recognized this problem and used only randomizations that had the same number of peaks as observed in the data . Quinn offered an alternative test that compared waiting times between peaks to the expectation of random events (a broken-stick distribution) . This test, he claimed, failed to demonstrate any evidence of periodicity in either the familial or the generic data . Unfortunately, he used an arbitrary definition of 'mass extinction' (either all stages with extinction intensities in the upper quartile of the data, or all peaks exceeding the mean intensity after log- linear adjustment for temporal trends) . His test appears to be sensitive to the number of points selected and could reject a moderately noisy sine curve if the number of points exceeded the number of cycles . Running Quinn' s test for different numbers of cycles or points would have presented difficulty in assessing the significance level for multiple tests .

2 . 1 2 Mass Extinction : Processes Quinn (1987) complained that Raup & Sepkoski (1984) did not calculate the joint significance level for the 49 independent tests that were conducted in assessing all periodicities between 12 and 60 million years (although Raup & Sepkoski did attempt to tackle this, albeit incorrectly) . Quinn claimed the joint significance level was only 39%, given a sig­ nificance of 99% for the fit of the 26 million year period . Tremaine (in Smoluchowski et al. 1986) cal­ culated the joint significance level to be 95 .4%, using a recomputed significance of 99 . 74% for the 26 million year period . Tremaine went on to argue, however, that random simulations run over the 1 2 6 0 million year band indicated a joint significance level of less than 90% for the 12 peaks of Raup & Sepkoski (1984) and less than 50% for the eight peaks of Sepkoski & Raup (1986) . But these results may have been sensitive to his assumption that variance in fit was directly proportional to period length in his tests . Raup & Sepkoski (1986) used Tremaine's procedure without this assumption and obtained joint significance levels greater than 95% . All of these tests and arguments have used a Poisson model of randomness as a basis of compari­ son . Lutz (1987) argued that this is not the only alternative in testing for periodicity . He tested Raup & Sepkoski's (1984) familial time series against models for Poisson distributions, 'noisy' period­ icities, and constrained episodicities (i . e . y distri­ butions in which the standard deviation in waiting times is less than the mean waiting time) . He found that the Poisson model could be rejected at the 95% significance level, but he could not distinguish be­ tween fits of noisy periodicities and of episodicities with variances less than 30% of mean waiting time (although it is not clear how sensitive these results are to selection of events and to errors in the time­ scale) . Lutz (1987) concluded that an exogenous forcing agent with clock-like behaviour was not necessary to explain the data . Stanley (1987) proffered a similar argument on qualitative grounds . He suggested that extinction events eliminate particularly vulnerable taxa and that there is a lag time after each event during which few vulnerable taxa are available for extinction . Thus, palaeontologically recognizable perturbations should be spaced more widely than expected from a Poisson distribution . The counter to this argument is that recovery times observed for most extinction events in the Mesozoic and Cenozoic are only one or two stages, which is within the lag time built into Raup & Sepkoski's randomization procedure .

177

It cannot be claimed that any of these arguments and counterarguments is decisive, and it is doubtful whether new, more accurate data could settle the matter (although more precise data would certainly promote better understanding of extinction in the fossil record) . A definitive settlement will be reached only if a clear agent of periodic extinction is discovered .

Possible causes o f periodicity Both terrestrial and extra-terrestrial mechanisms have been suggested as ultimate causes of period­ icity in extinction. The terrestrial mechanisms in­ volve hypothetical quasiperiodic processes in the deep Earth that lead to episodes of intense volcan­ ism . The extra-terrestrial mechanisms involve a var­ iety of observed and hypothesized astronomical clocks that might induce periodic cometary bom­ bardments of the Earth . Evidence that extra-terrestrial impacts might be important in periodic extinction come from two sets of observations (see also Section 2 . 12.2) : 1 Materials presumed to b e of impact origin (excess iridium, microtektites, and/or shocked mineral grains) are associated with several periodic extinction events, including the Cenomanian, Maastrichtian, Upper Eocene, and Middle Miocene . 2 Ages of terrestrial craters seem to exhibit a weak periodicity, involving 25 - 50% of impacts, that has a phase and period length (variously estimated at 27 - 32 million years) that are roughly congruent with the extinction periodicity (see Shoemaker & Wolfe in Smoluchowski et al. 1986) . The periodic impactors are presumed to be comets derived from the Oort Cloud at the outer fringes of the Solar System. It has been hypothesized that a gravitational perturbation from a body as small as four times Jupiter'S mass could induce a comet shower that would bring up to 109 comets into the inner Solar System; about 25 of these on average would strike the Earth over a 1 million year interval. Four mechanisms, all of which are flawed, have been suggested to produce such comet showers periodically (reviewed by Sepkoski & Raup 1986; Shoemaker & Wolfe in Smoluchowski et al. 1986) : 1 A dim binary companion to the Sun, dubbed 'Nemesis' . This small star is hypothesized to have a highly eccentric orbit with a mean revolution time of 26- 28 million years . At aphelion, it would pass through the Oort Cloud and induce a comet shower. However, a distant companion has never been ob-

178

2 The Evolutionary Process and the Fossil Record

served, and simulations indicate it would be un­ stable and easily stripped from its orbit by passing field stars and molecular clouds . 2 An unobserved tenth planet, usually called 'Planet X' . If it had a slightly eccentric orbit inclined to the plane of the Solar System, orbital precession could bring the perihelion into the solar plane twice every 52 - 56 million years, at which time the planet would scatter comets from the inner edge of the Oort Cloud . However, a tenth planet has never been observed, and it is not clear whether it would have sufficient mass to scatter enough comets to leave a recognizable periodic signature on Earth . 3 Oscillation of the Solar System perpendicular to the Galactic plane . This well known behaviour moves the Solar System every 31 - 33 million years through the dense plane of the Galaxy, where gravi­ tational encounters with molecular clouds might perturb the Oort Cloud . However, the oscillation is out of phase with the extinction periodicity, and it has been argued that the mass of the Galaxy is not sufficiently concentrated in the plane to affect any distinct periodicity over a 270 million year interval . 4 Quasiperiodic transit of the Solar System through the spiral arms of the Galaxy . During its galactic orbit, the Solar System passes through either two or four arms, where concentrated mass may perturb the Oort Cloud . However, the intervals between transits are either about 60 or 125 million years, which is much longer than the observed periodicity of extinction . Alternative hypotheses that deep-Earth processes could induce periodic extinction are based on two lines of evidence (see also Section 2 . 12 . 1 ) : (1) there is an arguable periodicity of around 30 million years in the frequency of reversals of the Earth's magnetic field, suggesting some kind of regularity in deep-Earth dynamics (Loper et al. 1988); and (2) several periodic extinction events are associated with immense volcanic deposits (e . g . the Siberian traps, Deccan traps, and Columbia River basalts), which were produced during major episodes of basaltic volcanism . Such episodes could release large quantities of particulates, sulphates, and carbon dioxide into the atmosphere, perturbing climate and inducing extinction . Loper et al. (1988) argued that major volcanic episodes would be quasiperiodic if they were caused by variation in the thickness of the thermal layer at the base of the mantle . Thickening of this layer through time could lead to dynamical ins ta-

bilities that would spawn mantle plumes and cause widespread basaltic volcanism . Release of the plumes would draw material from the thermal layer, re-establishing stability and thus limiting the dur­ ation of the volcanic episode . This hypothesis of terrestrial forcing challenges, but does not negate, a role for extra-terrestrial im­ pacts in producing the observed distribution of extinction events : coincidental impact during a vol­ canic episode could greatly amplify a biotic crisis . Both sets of hypotheses are consistent with the implication from periodicity that most Mesozoic ­ Cenozoic extinction events share a common ultimate cause . But, as Lutz (1987) noted, the deep-Earth mechanism is not strictly clocklike but would oper­ ate by constraining waiting times between f'vents to generate the non-random distribution that is seen in the fossil record of extinction .

References Fischer, A . G . & Arthur, M.A. 1977. Secular variations in the pelagic realm. In: H . E . Cook & P. Enos (eds) Deep-water carbonate environments . Special Publication of the Society of Economic Paleontologists and Mineralogists No . 25, pp . 19-50. Fox, W.T. 1987. Harmonic analysis of periodic extinctions. Paleobiology 13, 257- 271 . Hoffman, A. 1985 . Patterns of family extinction: dependence on definition and geologic time scale . Nature 315, 659 662 . Hoffman, A. & Ghiold, J. 1985 . Randomness in the pattern of 'mass extinctions' and 'waves of originations' . Geological Magazine 122, 1 - 4. Kitchell, J.A. & Pena, D . 1984 . Periodicity of extinctions in the geologic past: deterministic versus stochastic expla­ nations . Science 226, 689 - 692. Loper, D . E . , McCartney, K. & Buzyna, G. 1988 . A model of correlated episodicity in magnetic-field reversals, climate, and mass extinctions. Journal of Geology 96, 1 - 16 . Lutz, T . M . 1987. Limitations t o the statistical analysis of episodic and periodic models of geologic time series . Geology 15, 1 1 1 5 - 1 117. Noma, E . & Glass, A . L . 1987. Mass extinction pattern : result of chance . Geological Magazine 124, 319 - 322. Patterson, C. & Smith, A . B . 1987. Is the periodicity of extinc­ tions a taxonomic artefact? Nature 330, 248-25l . Quinn, J . F . 1987. On the statistical detection of cycles in extinctions in the marine fossil record . Paleobiology 13, 465 -478. Rampino, M.R. & Stothers, R.B. 1984. Terrestrial mass extinc­ tions, cometary impacts and the Sun's motion perpendicu­ lar to the galactic plane . Nature 308, 709 - 712. Raup, D.M. & Sepkoski, J.J., Jr. 1984. Periodicity of extinctions in the geologic past. Proceedings of the National Academy of Sciences, U. 5.A. 81, 801 - 805. Raup, D.M. & Sepkoski, J.J., Jr. 1986 . Periodic extinction of

2 . 13 Mass Extinction: Events families and genera. Science 23 1 , 833- 836. Sepkoski, J .J . , Jr. 1986. Global bioevents and the question of periodicity. In: O . Walliser (ed . ) Global bio-events, pp . 47-6 1 . Springer-Verlag, Berlin. Sepkoski, J.J., Jr. 1987. Is the periodicity of extinction a taxonomic artefact? Response . Nature 330, 251 -252 . Sepkoski, J.J., Jr. 1989 . Periodicity in extinction and the problem of catastrophism in the history of life . Journal of the Geological Society of London 146, 7 - 19. Sepkoski, J .J . , Jr. & Raup, D . M . 1986. Periodicity in marine

179

extinction events . In : D.K. Elliott (ed . ) Dynamics of extinction, pp. 3 - 36 . Wiley, New York. Smoluchowski, R . 5 . , BahcalI, J . N . & Matthews, M . S . (eds) 1986. The galaxy and the solar system . University of Arizona Press, Tucson . Stanley, S.M. 1987. Extinction . Scientific American Books, New York. Stigler, S . M . & Wagner, M.J. 1987. A substantial bias in non­ parametric tests for periodicity in geophysical data. Science 238, 940- 945 .

2 . 13 Mass Extinction: Events

2 . 1 3 . 1 Vendian M . A . S . McMENAMIN

Introduction The earliest known, reasonably well documented mass extinction is of Vendian age, and seems to have occurred in the middle part of the Vendian, about 650 Ma. The severity and timing of this ex­ tinction is somewhat obscured by the difficulty of obtaining precise dates for Vendian sediments . Also, some losses of Vendian diversity appear to be the continuation of declines that began before the be­ ginning of the Vendian, such as the loss of many different types of stromatolites .

Micro-organisms Stromatolites reached a peak in diversity (nearly 100 recognized taxa) in the Late Riphean (c. 850 Ma) . Following this acme, stromatolites underwent a precipitous decline (see also Section 1 .5) starting in the second half of the Late Riphean and con­ tinuing through the Vendian . Stromatolite diversity bottomed out at less than 30 taxa by the beginning of the Cambrian . Although this decline does not necessarily represent the extinction of any of the individual microbial species that participated in the formation of stromatolites, it does indicate that the conditions became much less favourable for many formerly successful types of benthic microbial communities . For example, well formed specimens of the conical Proterozoic stromatolite Conophyton

are unknown after the Vendian. The advent of burrowing and grazing metazoans, and disturbance to microbial mats as a result of their activities, has been hypothesized as the factor responsible for the decline of stromatolites . Individual taxa of benthic microbial organisms (Section 1 .2), represented by delicate unicells and filamentous chains of cells preserved in chert, seem to have been largely unaffected by extinction during the Vendian, although it is difficult to recognize taxonomic turnover in floras consisting primarily of morphologically simple coccoidal and filamentous microbes . This problem is further compounded by the fact that fossilized benthic microbiotas are rare after the beginning of the Cambrian; apparently the conditions necessary for fossilization of microbes in chert became much less common after the end of the Vendian . A different situation exists with acritarchs, a het­ erogeneous group of organic-walled microfossils recovered from sediment by acid maceration . By comparison with modem dinoflagellate cysts, most acritarchs are thought to represent the resting stages of planktic, eukaryotic marine algae (Section 1 . 7. 2) . Both within-flora and total taxonomic diversity of these planktic microfossils underwent a severe de­ cline during the Middle to Late Vendian, which Vidal & Knoll (1982) regarded as indicative of major extinctions in the eukaryotic phytoplankton . Diag­ nostic acritarch taxa such as Trachysphaeridium laufeldi and the distinctively striate Kildinella lopho­ striata (Vidal & Knoll 1982) disappeared by the Middle Vendian . These distinctive Late Riphean - Early Vendian acritarchs were succeeded by a depauperate flora typified by Bavlinella faveolata (an acritarch that

180

2 The Evolutionary Process and the Fossil Record

resembles the existing colonies of spherical cyano­ bacteria called chroococcaleans) and the ribbon­ shaped vendotaenid algae . The sediments containing this depauperate flora also have curious­ ly large amounts of organic matter (sapropel) derived from the burial of acritarchs and other organic-walled objects . The re-radiation of the plank­ ton from this low-diversity interlude was slow . Acritarch diversity in most stratigraphic sections did not recover to Early Vendian levels until well into the Lower Cambrian, when very spiny forms such as Skiagia became abundant (but see Zang & Walter 1989) .

A

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Metazoans The soft-bodied fossils of the Ediacaran fauna are generally thought to be metazoans (Section 1 .3) . Frondose or leaf-like Ediacaran forms such as Charnia and Charniodiscus are known throughout the world in sediments of Vendian age . Some of these organisms attained sizes of up to one metre in length . The second half of the Vendian (the Kotlin Horizon) is marked by local extinction on the Russian Platform of many of these large, distinctive soft-bodied creatures . Possibly coincident with the decline in phytoplankton diversity, Late Vendian metazoan faunas of the Russian Platform were re­ duced to rare problematic forms of medusoids and small trace fossils (Fedonkin 1987; Sections 1 . 3, 1 . 5) . The Ediacaran fauna seems to have died off by ' the end of the Vendi an (the top of the Rovno Horizon of the Siberian Platform), although a few of these soft-bodied forms may have survived into the Early Cambrian. Seilacher (1984) argued that the end of the Vendian witnessed a mass extinction of the soft-bodied Ediacaran forms, and that these extinc­ tions were real and were not an artifact of preser­ vation . It must be noted, however, that the intensity of burrowing increased greatly in the terminal Vendian. The trace fossils at this time became more complicated, deeper and larger, indicating an in­ crease in the dimensions of infaunal animals . This development may have reduced the potential for preservation of soft-bodied animals . The Late Vendian increase in burrowing intensity was accompanied by an explosion in the diversity of trace fossils . Numerous new ichnotaxa appeared that have ranges continuing through most or all of Phanerozoic time . Of the dozens of new ichnogenera that first appeared in the Vendian, only six became extinct by the end . Of these, Neonoxites, and Palaeo­ pascichnus were horizontal grazing or very shallow

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deposit feeding traces (Fig. 1 ) . If there was indeed a mass extinction at the end of the Vendi an, it was overshadowed by the metazoan diversification occurring at this time . The study of Vendian extinctions is hampered by a paucity of well preserved macrofossils . Neverthe­ less, the disappearance of acritarchs suggest that the Middle Vendian was marked by a mass extinc­ tion event that rivalled in magnitude the better known mass extinctions occurring later in the Phanerozoic . This Middle Vendian acritarch extinc­ tion event was linked to the Varangian glaciation by Vidal & Knoll (1982), who invoked climatic cool­ ing as a causal mechanism. More evidence is needed to clarify the timing, severity, and possible climatic control of these extinction events . Of particular in­ terest is the unresolved question of whether global metazoan mass extinctions occurred in the Vendian, and whether or not they were coincident with the phytoplankton extinctions .

References Fedonkin, M.A. 1987. The non-skeletal fauna of the Vendian and its place in the evolution of metazoans . Nauka, Moscow (in Russian).

181

2 . 13 Mass Extinction: Events Seilacher, A. 1984. Late Precambrian and Early Cambrian Metazoa: preservational or real extinctions? In: H.D. Holland & A.F. Trendall (eds) Patterns of change in Earth evolution, pp. 159 - 168. Springer-Verlag, Berlin. Vidal, G. & Knoll, A.H. 1982. Radiations and extinctions of plankton in the late Proterozoic and early Cambrian. Nature 297, 57-60. Zang, W.L. & Waiter, M . R. 1989. Late Proterozoic plankton from the Amadeus Basin in central Australia. Nature 337, 642 - 645 .

2 . 1 3 . 2 End-Ordovician P . J . BRENCHLEY

Brachiopods. Thirteen families of brachiopods be­ came extinct at or near the Ordovician- Silurian boundary . Of the 27 families which crossed the boundary, nine showed a marked decline in abun­ dance (Sheehan 1982) . Amongst the rich brachiopod faunas of the Ashgill of northwest Europe, 25% of genera disappeared at the top of the Rawtheyan and another 40% at the top of the Hirnantian (Fig. 1). Graptolites. The diversity o f graptolite species de­ creased from a high point in the Late Caradoc to a nadir in the Climacograptus extraordinarius and Glyp­ tograptus persculptus zones, when the total world graptolite fauna consisted of only a few genera . Primitive echinoderms. The diversity of cystoid, edrio­

Introduction About 22% of all families became extinct in the Late Ordovician, which makes this one of the largest episodes of mass extinction (Raup & Sepkoski 1982) . Although there were some extinctions throughout the Ashgill, the main phase of extinction was in the Late Ashgill . The Late Ordovician extinctions can­ not be related to a single stratigraphic level, but occurred in at least two steps. One phase coincided with the start of a major regression at the end of the Rawtheyan (the penultimate stage in the Ashgill) and a second phase coincided with a transgression .at the end of the Hirnantian (the last Ashgill stage), about 1 -2 million years later (Brenchley 1984) . There may in addition have been some extinctions throughout Hirnantian times . The two major phases of extinction have been best documented from clastic sequences in Europe . Upper Ordovician extinctions of comparable magnitude are known from carbonate sequences in North America but have not been clearly differentiated into two phases .

Extinction patterns

asteroid, and cyclocystoid families declined sharply in the Late Ashgill . The sharpest drop in num­ bers of cystoid genera in the families Diploporita and Dichoporita was at the Rawtheyan - Hirnantian boundary, when the rich and varied Rawtheyan fauna with 26 genera was reduced to a small but distinctive Hirnantian fauna with only eight. Most of the latter fauna apparently disappeared at the end of the Hirnantian .

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182

2 The Evolutionary Process and the Fossil Record

Conodonts. The mainly clastic Hirnantian se­ quences of Europe have yielded very few species of conodonts, even where collecting has concentrated on the more promising limestone horizons. In the carbonate sequences of North America di­ verse conodont faunas declined a little in the Gamachian and disappeared almost completely at the Ordovician - Silurian boundary. Chitinozoa, acritarchs, and ostracodes. All three groups show major decreases in diversity and changes in taxonomic composition at or near the Ordovician ­ Silurian boundary .

Corals. The best data for the Late Ordovician show that c. 50 of the 70 tabulate and heliolitoid gen­ era became extinct in Late Ordovician times . It is not clear whether this was an end-Rawtheyan or Hirnantian extinction . Following the first wave of extinction at the end of the Rawtheyan there was a residual fauna, domi­ nated by brachiopods, which is usually referred to as the Hirnantia fauna . This fauna is unusually cosmopolitan and appears to have ranged from cir­ cumpolar to sub-tropical latitudes, though it was not well developed in the carbonate environments of tropical regions. The Hirnantia fauna is commonly considered to have been a relatively cool water fauna . The second wave of extinction at the top of the Hirnantian (top Gamachian in Canada) was rela­ tively modest in the clastic sequences of Europe . Several elements of the Hirnantia fauna disappeared at this level, and coral and ostracode faunas may have been heavily depleted . Coral-stromatoporoid reefs which occur at the top of the Hirnantian are rare or absent in the lower levels of the succeeding Silurian . In North America the diversity of brachiopods, trilobites, conodonts, acritarchs, and ostracodes greatly diminished at the end of the Ordovician (Lesperance 1 985 ), but because the detailed strati­ graphy is uncertain the extinctions could be Early or Late Hirnantian . Environmental changes In most shelf sequences there is a change of facies at the Rawtheyan - Hirnantian boundary, reflecting the start of the regression which reached its maxi­ mum in the Middle or Upper Hirnantian . The re­ gression partially drained many clastic shelves leaving a variety of shallow-marine sandy deposits .

A major part of the world's carbonate platforms became exposed with widespread development of karst surfaces and disconformities . At the top of the Hirnantian there is generally a sharp change in facies indicating a rapid trans­ gression . In many clastic sequences the shallow­ marine rocks of the Upper Hirnantian are overlain by black graptolitic shales . In carbonate regions there is a progressive return to more offshore carbonate facies . I t has been estimated that the regression in­ volved a fall in sea-level of 50- 100 m (Fig . 2) . In several Hirnantian sequences there is some evi­ dence of fluctuations of sea-level (two to four re­ gressions) but the pattern is not clear on a global scale .

Causes The cause or causes of the extinctions are debatable . The stepped nature of the extinctions makes an extra-terrestrial cause, such as meteorite impact, unlikely . Furthermore no iridium anomaly was discovered in detailed investigations of the Ordovician- Silurian stratotype at Dob' s Linn or in the carbonate sequence of Anticosti Island . The very precise correlation between the disappearance of faunas in many sections and the first evidence of regression makes it likely that the extinctions were related to contemporaneous environmental changes such as the following : 1

Sea-level changes. The fall in sea-level during the Hirnantian would have drastically reduced the size of continental shelves and platforms and hence the habitable area for shelf benthos. Many very exten­ sive platforms (N. America, Baltica and the Russian Platform) were covered by shallow seas during most of the Ordovician so a sea-level fall of tens of metres would have had a profound effect . The main argument against a major role for sea­ level change in causing extinctions is that the faunal changes were concentrated at the Rawtheyan ­ Hirnantian boundary while the regression appears to have continued throughout the early part of the Hirnantian . The second phase of extinction at the top of the Hirnantian coincides with a rise in sea­ level, and consequently a potential increase in hab­ itable area. However, following the transgression, black shales were deposited on many clastic shelves, indicating widespread anoxic or dysaerobic con­ ditions hostile to benthic faunas (see also Section 2.12.1).

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Although changes in sea-level may have had some effect on the shelf benthos they do not satis­ factorily account for the major extinctions amongst the plankton . 2

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extent of upper Ordovician continental glaciation on Gondwanaland, and the occurrence of marine tilloids peripherally, for a very substantial extension of arctic and subarctic conditions in the Hirnantian . On the other hand, tropical carbonate environments survived at the same time in equatorial latitudes. There might well have been a substantial reduction in the area of temperate seas and some restriction of tropical regions which could account for the reduction in diversity of microplankton and grapto­ lite s . The widespread distribution of the Hirnantia fauna might be related to the spread of cool water, which could even have impinged on formerly trop­ ical areas during major phases of glaciation . The second phase of extinction at the top of the

Hirnantian should have been at a time of rising temperature so it is unlikely that this phase of extinction was the result of changing climate . 3

Oceanic overturn. It has been suggested that dur­ ing periods of climatic change the stability of weakly stratified ocean waters might be disturbed, and that they could overturn bringing 'unconditioned' biologically-toxic bottom water to the surface (Wilde & Berry 1984) . Such overturns might occur either during a period of climatic deterioration, when cold water from high latitudes intruded below weakly stratified ocean waters, or during times of climatic amelioration . The model of oceanic overturn has several attrac­ tions, as it can account for the coincidence of the two phases of extinction with times of maximum climatic change, and for extinction of both plankton and shelf benthos . Furthermore, the effects of over­ turn would have been rapid, which accords with the disappearance of faunas at precise levels in

2 The Evolutionary Process and the Fossil Record

184

many sections. Unfortunately no evidence of oceanic overturn has yet been detected in the sedimentary record . In summary, changes in both temperature and sea-level, for which there is good evidence, might have played a significant role in the faunal extinc­ tions . A related oceanic overturn could have been important, but remains hypothetical .

References Brenchley, P.J. 1984 . Late Ordovician extinctions and their re­ lationship to the Gondwana glaciation . In : P.J. Brenchley (ed . ) Fossils and climate, pp . 291 -315. John Wiley & Sons, Chichester. Lesperance, P.J. 1985. Faunal distributions across the Ordovician - Silurian boundary, Anticosti Island and Perce, Quebec, Canada . Canadian Journal of Earth Sciences 22, 838- 849. Raup, D . M . & Sepkoski, J . J . , Jr 1982 . Mass extinctions in the marine fossil record . Science 215, 1501 - 1503 . Sheehan, P.M. 1982 . Brachiopod macroevolution at the Ordovician -Silurian boundary. Proceedings of the Third North American Paleontological Convention 2, 477-481 . Wilde, P. & Berry, W.B.N. 1984. Destabilisation of the oceanic density structure and its significance to marine 'extinction' events . Palaeogeography, PalaeoC/imatology, Palaeoecology 48, 143 - 162.

2 . 1 3 . 3 Frasnian - Famennian G . R . McGHE E , Jr

Extinction patterns The massive deterioration in ecosystems which occurred throughout the world during the Frasnian - Famennian event can be described cor­ rectly as catastrophic in effect (McLaren 1982) . Frasnian ecosystems were ecologically very di­ verse and equitable in structure . Early Famennian ecosystems, in contrast, were impoverished in eco­ logical diversity and in overall species richness. The effect of the biotic crisis can easily be seen in the 'bottleneck' constriction of ecological complexity which occurred in the Appalachian region of eastern North America . There the diverse Frasnian eco­ system is replaced by an ecologically depauperate Famennian ecosystem proportionately over­ dominated by reduced species numbers of brachio­ pods, bivalves, and glass sponges (McGhee 1982) .

The analysis of the fossil remains of organisms around the globe which perished during the extinction event, as well as those which survived, reveals the following ecological patterns:

Latitudinal effect. Tropical reefal and perireefal marine ecosystems were particularly hard hit . The low-latitude, geographically widespread and massive stromatoporoid-tabulate reefal ecosystems vanished, and perireefal rugose coral­ tabular stromatoporoid bioherms were deci­ mated. The stromatoporoids suffered a severe reduction in biomass, but they did not become extinct nor did they totally lose their reef-building potential (Steam 1987) . Post-Frasnian stromato­ poroid structures are of small dimensions, and are generally found in the warm water equatorial region of the Palaeotethys. Famennian stromato­ poroids found outside this area are generally labechiids, which are believed to have been bet­ ter adapted to cool water than the majority of Frasnian species, which were tropical and low­ latitude in distribution . Differential survival of high-latitude, cool-water adapted species is also exhibited by the brachio­ pods, which were the dominant form of shelly ani­ mal in Frasnian benthic ecosystems (Copper 1986) . Of the total brachiopod fauna, approximately 86% of Frasnian genera did not survive into the Famen­ nian . However, 91% of brachiopod families whose species were generally confined to low-latitude, tropical regions perished in the extinction event, in contrast to a loss of 27% of those families with species which ranged into high-latitude, cool-water regions. Other elements of the marine benthos which exhibit latitudinal patterns of survival include the foraminifera . They suffered major losses in species diversity with the substantial reduction which oc­ curred in the area of the global belt of carbonate sedimentation . Species of the high-latitude regions differentially survived the event; species of the cool­ water Siberian realm expanded their geographical ranges into low-latitude regions with the latitudinal contraction in the range of Palaeotethys species .

Bathymetric effect. In general, shallow-water marine ecosystems were much more severely affected during the Frasnian - Famennian interval than deeper-water systems . The bathymetric selectivity in extinction is seen most dramatically within the rugose corals, a group which suffered a massive loss in biomass . Only 4% of the shallow-water species

2 . 13 Mass Extinction: Events survived . Deeper-water species suffered a 60% ex­ tinction in their numbers, and while this reduction was severe it pales in comparison with the 96% loss of species in the shallow waters . The decimation of the shallow-water corals was actually more severe than that of the stromatoporoids (Steam 1987) . A particularly intriguing bathymetric pattern of selective extinction and diversification occurs across the Frasnian - Famennian boundary in the Appala­ chian marine ecosystems of eastern North America . Simultaneously with the extinction of many shallow-water benthic species, the hyalosponges (glass sponges) migrated from deeper water into the shallows and underwent a burst of diversifica­ tion in species numbers . Modern glass sponges are generally found in water depths in excess of 200 m, and are considered to be better adapted to cold er waters than most other invertebrate species. Blooms in other siliceous organisms, most notably the radio­ larians, are also reported during the Frasnian ­ Famennian interval .

Habitat effect. A marked habitat effect in selective survival can be observed in the Devonian fish groups which included both marine and freshwater species . Only 35% of marine placoderm species survived, in contrast to 77% of those which lived in freshwater. A similar pattern occurs in the acan­ thodian fishes : only 12% of marine species survived, in contrast to 70% of freshwater species . A key environmental parameter which differen­ tiates the two habitat regions (other than salinity) is temperature . In general, freshwater species are adapted to seasonal and diurnal fluctuations in tem­ perature, in contrast to those species in temperature­ buffered shallow-water marine regions . The differential survival of freshwater fish may reflect their greater tolerance to temperature changes . Other elements o f the terrestrial ecosystem appear to have been unaffected by the event. Floras exhibit no major disruptions, and plant biomass pro­ ductivity appears to have been unchanged, or even perhaps enhanced, during the Frasnian ­ Famennian interval . Within the shallow-water marine benthos, epi­ faunal filter-feeding organisms appear to have been most affected by the extinction event; infauna and detritus feeders were relatively unaffected . In common with other extinction events, the up­ per oceanic water habitat of the marine plankton was massively disrupted . Approximately 90% of the preservable phytoplankton was affected, and

185

massive biomass reductions also occurred among the zooplankton .

Summary. The ecological signature preserved in the fossil record of the Frasnian - Famennian extinction event appears to indicate a significant drop in global temperatures during the crisis interval . The deci­ mation of low-latitude tropical reef ecosystems and of warm-water shallow marine faunas, combined with the relatively higher survival of high-latitude faunas, deep-water faunas, and terrestrial fauna and flora, seems most compatible with lethal tempera­ ture decline at a global level . At the local and re­ gional level the extinction event doubtless records additional local environmental factors .

Evolutionary dynamics The precise timing of the Frasnian - Famennian ex­ tinction event is still uncertain . Present evidence, however, indicates that extinction rates were elev­ ated above average during a geologically significant span of time during the latter half of the Frasnian, for a period of perhaps 3-4 million years (Fig. 1 ) . There appears to have been n o single synchronous extinction peak shared by all species, but a series of stepwise extinctions of different species groups. It has been consistently observed, however, that a marked drop in standing species diversity occurred at the very end of the Frasnian . The fact that extinc­ tion rates were elevated above average for a signifi­ cant period of time before the terminal Frasnian suggests that the drop in species diversity at the Frasnian -Famennian boundary was not a simple function of extinction rate magnitudes (McGhee

1982) . In the analysis of ecosystem evolution it is often misleading to consider the pattern and timing of extinction rates alone . Species diversity is a function of the relationship of two evolutionary variables : the rate a t which species were lost from the system (extinction rate), and the rate at which new species were added (origination rate) . While either rate alone is of considerable interest, the evolutionary behaviour of the total ecosystem can best be charac­ terized by the sign and magnitude of species diver­ sity changes (the turnover rate, i . e . origination rate minus the extinction rate) . If origination and extinc­ tion rates were of equal magnitude, the ecosystem was in a state of dynamic equilibrium with no diversity change . Where origination exceeded ex­ tinction (positive turnover rates), the system was

0 4-------�--� F ras n i a n Famen n i a n 374

367

360

G e o l o g ical t i m e (1 0 6 yrs) Fig. 1 Elevated extinction rates during the Middle and Late Frasnian exhibited by brachiopods from the Appalachians, V.5.A. (solid line) contrasted with the Vrals, V.S.5.R. (dashed line) . Extinction rate metric is the number of species extinctions (E) per million years (i', t) .

diversifying, whereas if extinction exceeded orig­ ination (negative turnover rates) the system was losing species diversity . Marine ecosystems appear to have been flourish­ ing (in terms of standing species diversity) during the interval of time characterized by some of the highest extinction rates which occurred in the latter half of the Frasnian . This phenomenon is due to the fact that species origination rates were even higher per time interval than the corresponding extinction rates. This pattern of relative origination - extinction rate magnitudes reversed abruptly during the latest Frasnian, precipitating a rapid loss of species diver­ sity (Fig. 2) . Extinction rates in many cases remained the same, or actually declined in some, but species

- 8 4-----�r---� F ras n ia n Famen n i a n 374

367

360

Geolog i c a l t i m e ( 1 0 6 yrs) Fig. 2 Species turnover rates for brachiopods from the Appalachians, V.5.A. (solid line) and the Vrals, V . 5 . 5 .R. (dashed line) during the Frasnian- Famennian interval. A sharp negative pulse in turnover rates occurs in both regions at the very end of the Frasnian, signalling a severe and rapid loss of species diversity in this interval of time . Turnover rate metric is the change in the number of species ( i', S) per million years (i', t) .

turnover rates became sharply negative (Fig . 2) . Whether extinction rates were rising or falling, it was the decline in species originations which drove species turnover rates sharply negative at the very end of the Frasnian . Thus, while there was no single synchronous extinction rate pulse during the Frasnian, the eco­ system did exhibit a rather abrupt and massive drop in species diversity in the terminal Frasnian . In understanding the ultimate cause of the extinc­ tion event the most important question may not be what triggered the elevated extinction rates, but what was the inhibiting factor that caused the cessation of new species originations .

187

2 . 13 Mass Extinction: Events References Copper, P . 1986. FrasnianfFamennian mass extinction and cold-water oceans. Geology 14, 835 - 839. McGhee, G . R . , Jr. 1982 . The Frasnian - Famennian extinction event: a preliminary analysis of Appalachian marine ecosystems . Special Paper of the Geological Society of America 190, 491 -500. McLaren, D.J. 1982 . Frasnian-Famennian extinctions . Special Paper of the Geological Society of America 190, 447-484. Steam, C . W. 1987. Effect of the Frasnian - Famennian extinc­ tion event on the stromatoporoids . Geology 15, 677- 679 .

2 . 13 . 4 End-Permian D . H . E RWIN

Introduction During the latest Permian 54% of all marine families became extinct (Table 1), as did 83% of all marine genera (Sepkoski 1986) . Several authors have esti­ mated that as many as 90-96% of all durably­ skeletonized marine invertebrate species became extinct (e .g. Sepkoski 1986 ) . This extinction was the most severe of the Phanerozoic and eliminated twice as many families as the second largest, the end­ Ordovician mass extinction (Section 2 . 13 .2) . Many major taxa were eradicated or declined drastically in diversity, eliminating the shallow-water, sessile, epifaunal, brachiopod -bryozoan -pelmatazoan echinoderm communities which dominated the Palaeozoic. This permitted the expansion of the mobile, infaunal, molluscan-dominated communi­ ties which dominated the post-Palaeozoic. The effects of the extinction on land are less clear, but extinc­ tions and changes in faunal dominance occurred in both terrestrial vertebrates and plants throughout the Permian . Despite its magnitude and significance, analysis of the patterns and causes of the extinction has been hampered by the restricted number of marine sec­ tions of latest Permian age . The number of well­ studied sections has increased recently, particularly in South China and elsewhere in the Tethyan region . However, facies changes at the boundary indicate that no continuous Late Permian - Early Triassic sections have been discovered . The assembly of the supercontinent Pangaea was largely completed with the collision of the

Table 1 Extinction percentages for 17 major groups of marine families during each series of the Permian . Families not resolved to series were not used in the analysis . A Asselian, S Sakmarian, L Leonardian, G Guadalupian, D Dzulfian. (Data from Sepkoski 1982 . ) =

=

=

=

=

Percentage extinction Marine family

A

S

L

G

D

Foraminifera Porifera Tabulata Rugosa Gastropoda Bivalvia Cephalopoda Other Mollusca Other Arthropoda Ostracodes Bryozoa Brachiopoda Crinoidea Other Echinodermata Conodonta Other taxa Marine vertebrates

0 0 0 0 0 0 17 0 0 4 10 0 0 5 0 0 0

0 0 14 6 0 3 0 17 0 8 4 3 16 5 20 0 0

3 18 15 38 15 2 20 40 21 8 4 12 5 5 0 0 0

6 24 42 62 25 12 43 33 33 35 23 34 93 37 20 9 39

38 10 100 100 11 11 47 0 25 29 65 71 0 8 25 3 0

Kazakhstan, Tarim, and Siberian blocks in the Late Carboniferous and the accretion of this unit to the Russian platform by the end of the Artinskian Stage (Fig . 1 ) . The North China block collided with Kazakhstan in the latest Permian . The South China block closely approached the North China block in the latest Permian but rotation and accretion of the two blocks was not completed until the Late Triassic or Early Jurassic . (Considerable movement and ro­ tation occurred between tectonic blocks during the Permian . Consequently, palaeocontinental recon­ structions are poorly constrained until the Late Triassic . ) The Late Carboniferous - Early Permian glaciation in Gondwanaland ended during the Asselian ­ Sakmarian as the South Pole moved off the continent and the formation of Pangaea led to increased temperatures and seasonality (see Fig . 2 for time­ scale) . Continuing climatic oscillations into the Late Permian are suggested by sea-level fluctuations on a 2 - 2 . 5 million year cycle . Scattered reports of Late Middle to Late Permian glaciation, however, involve only restricted mountain glaciations . Global warm­ ing continued into the Triassic and there is no evidence for widespread cooling or glaciation during the Late Permian .

2 The Evolutionary Process and the Fossil Record

188 ,/

Fig. 1 Palaeocontinental reconstruction for the Late Pennian . AF Africa, AM Asia Minor, ANT Antarctica, AUS Australia, E Europe, I India, K Kazakhstan, NA North America, NCB North China block, S Siberia, SCB South China block, T Tarim. (From Lin et al. 1985 . Reprinted by permission Rom Nature vol. 313 pp . 444 - 449 . Copyright © 1985 Macmillan Magazines Ltd . =

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The increased temperatures and seasonality as­ sociated with the formation of Pangaea are indicated by evaporites and red beds. As continents become more exposed during a regression, the ameliorating effects of the ocean (due to the high heat capacity of water) decline, climates become more severe, and seasonality increases, a condition described as in­ creased continentality or inequability (Valentine & Moores in Logan & Hills 1973; Jablonski 1986) . The concentration of land area in one unit exacerbated the trend, leading to high seasonality in continental interiors . The effects were not limited to continental interiors . Storm activity, particularly monsoons in the Tethyan realm, and consequent disturbances in shallow-marine ecosystems, increased . The largest Permian evaporite deposits are of Kungarian age, coinciding with the initial formation of Pangaea, although these are dwarfed by later Triassic de­ posits . Finally, a sharp marine regression occurred at the end of the Permian .

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2 . 13 Mass Extinction: Events Extinction patterns Taxa which became extinct include tabulate and rugose corals, conularids, eurypterids, leperditiid ostracodes, several gastropod groups, goniatitic am­ monites, orthid and productid brachiopods, blas­ toids, inadunate, flexible, and camerate crinoids, and the few remaining trilobites (Table 1 ; Fig. 3) . A number of other groups suffered sharp drops in diversity, including the cryptostomate and treposto­ mate bryozoans, foraminifera, ammonoids and fish . Reefs were eliminated and tropical ecosystems in general were severely affected. Jablonski (1986) ana­ lysed survival patterns of articulate brachiopods and noted that 75% of the families confined to the tropics became extinct, while only 56% of extra­ tropical families died out . All fusilinid foraminifera and 54% of all foraminiferan families became ex­ tinct, including both planktic and benthic taxa . In general the zooplankton, sessile filter feeders, and the high-level carnivores (ammonoids and fish) were the most strongly influenced trophic groups . The diversity history o f marine vertebrates paral­ lels that of invertebrates, with the decline beginning in the Guadelupian and accelerating in the Dzulfian . Elasmobranchs, Holocephali and marine Chondros­ tei and Holostei follow this pattern. Freshwater and euryhaline fish and amphibians, however, reach a diversity low in the Leonardian and appear to be diversifying across the boundary. Sepkoski identified three distinct assemblages of taxa during the Phanerozoic, each with character­ istic diversity maxima (Section 1 .6) . His Palaeozoic evolutionary fauna includes the groups which domi­ nated the Palaeozoic: articulate brachiopods, crin­ oids and other pelmatazoan echinoderms, and bryozoans . These taxa suffered disproportionate ex­ tinction during the end-Permian, with a 79% fam­ ilial extinction, while bivalves, gastropods, some arthropod taxa, and others which constitute the Mesozoic - Cenozoic evolutionary fauna declined 27% . This differential extinction pattern contributed to the development of burrowing, infaunal, molluscan-dominated communities in the post­ Palaeozoic. The Permian extinction produced a large number of 'Lazarus taxa' : taxa which disappear from the record during the Late Permian, only to reappear in the Triassic (Jablonski 1986) . As Batten (in Logan & Hills 1973) noted, 'Palaeozoic' -aspect gastropods are better represented in the Triassic than in the latest Permian . The number of Lazarus taxa indicates that the record across the boundary is too fragmentary

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and sparse to accurately reflect the rate and duration of the extinction . Furthermore, many groups which first appear in the Triassic, including zygopleurid gastropods and scleractinian corals, are clearly de­ scended from Palaeozoic ancestors but with a sig­ nificant gap between ancestor and descendant. The restricted number of sections, the paucity of the fossil record, and the obvious sampling problems make it difficult to determine whether the extinction began in the Guadelupian or was restricted to the Dzulfian - Changhsingian (see also Jablonski 1986) . Preliminary generic diversity data (Fig . 4) show the extinction peak in the Guadelupian, although this may be a preservational artifact (Sepkoski 1986) . An indirect method of determining the duration of an extinction event is to analyse the replacement ratio, or the ratio of originations to extinctions (OIE

190

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is accentuated by an unusual upland fauna from the

2 . 13 Mass Extinction: Events Beaufort Series (Dzulfian) of South Africa with a large number of endemic families . If mass extinc­ tions are characterized as short-term extinction episodes significantly above background rates (Jablonski 1986), the vertebrate extinctions at the close of the Permian are merely one of a series of extinctions and replacements . There is no compel­ ling evidence of a mass extinction . Permian floras included a mesic, equatorial as­ semblage of broad-leaved pteridosperms, cordaites, and pecopterid ferns, the Glossopterid flora domi­ nated by pteridosperms, and an endemic Asiatic (Angaran) flora of cordaites . Vascular plant diversity dropped by 50% from the Early Permian to the Middle Triassic (Fig. 5A; Knoll in Nitecki 1984) . The Palaeophytic floras were replaced briefly by a mixed flora of Palaeophytic and Mesophytic affinities be­ fore development of a truly Mesophytic flora of conifers, cycads, ginkgoes, and new groups of pteri­ dophytes and pteridosperms . Local transitions took 5 million years or less but the global change occurred diachronously over 25-30 million years . Knoll (in Nitecki 1984) attributed these changes to the disap­ pearance of warm, equable climates in low latitudes as the glaciation ended, and to the spread of drier climates during the coalescence of Pangaea . The drier climates allowed conifers to invade the low­ lands and replace archaic pteridosperms and pteri­ dophytes . Despite the transition between floral types, there is no evidence of a major extinction event at the close of the Permian . Olson (in Silver & Schultz 1982) discounted a link between the end of the Permo-Carboniferous glaciation and vertebrate diversity patterns, but such a link now seems likely . Vertebrate diversity may have responded directly to climatic change or have been indirectly affected through restructuring of plant communities .

The Permo-Triassic boundary The total number of marine Permo-Triassic bound­ ary sections remains few, but good exposures are present in south China, the Salt and Surghar Ranges of Pakistan, Malaysia , Kashmir, northern Iran and southern Soviet Armenia, and east Greenland . Un­ fortunately the completeness of several of these sections is questionable and a widespread discon­ formity may be present . A di stinctive fauna combin­ ing Permian-type brachiopods and Triassic-type bivalves and ammonoids is widespread in South China and occurs in Kashmir, east Greenland, Dzulfia, and Pakistan (Sheng et al . 1984). The Permian elements are similar to a siliceous facies

191

assemblage lower in the section, but individual species are frequently dwarfed. This fauna is de­ posited in units 0.2-2.0 m thick with three distinct assemblages (Fig . 2) . In south China 'mixed fauna bed l' is a 10 cm thick yellowish or greenish-brown shale containing numerous Permian-type brachio­ pods and Triassic-type cephalopods . Bed 2 is a 20- 30 cm marly dolomite with Permian brachio­ pods and a few foraminifera . Mixed-fauna beds 1 and 2 appear to be equivalent to the Otoceras Zone, the lowest zone of the Triassic . Bed 3 is a greenish shale of variable thickness containing the Triassic bivalve Claria and cephalopod Ophiceras . Few Permian taxa are present (Sheng et al . 1984) . Earlier work suggested that the beds were formed by post-depositional mixing, but recent analysis of their sedimentology, preservation, and areal extent suggests that the mixed faunas are real . However, the abrupt facies shifts present in the three beds signifies a disconformable rather than strictly con­ formable boundary . The best evidence for a rapid mass extinction at the close of the Permian is the disappearance of seven genera and 22 species of Permian brachiopods in beds 1 and 2, which actualIy occurs in the lowest Triassic!

Causes Suggested causes for the end-Permian extinction have included trace element poisoning, regression­ induced species- area effects, cosmic radiation, high temperatures, global cooling, salinity changes, trophic-resource fluctuations, tectonically-induced changes in marine faunal provinces, and extra­ terrestrial impact . The range of explanations reflects the scarcity of information on latest Permian - earliest Triassic faunas, and the variety of geological events during the Late Permian . Several suggestions can be disposed of quickly . Cosmic radiation, long a favourite of O . Schinde­ wolf, does not penetrate the surficial ocean layer and cannot affect benthic organisms . Salinity changes would have been greater in the Middle Permian and Middle Triassic, when the maj or evaporite deposits were formed, than in the Late Permian . The possibility of an extra-terrestrial im­ pact, and thus a connection with the Cretaceous ­ Tertiary extinction, was fuelled by reports of an iridium anomaly of 2.0 ppb in Chinese boundary sections (Xu et al . 1985) but attempts to reproduce the results have failed (Clark et al. 1986) . At present there is no evidence for an impact event at this boundary .

192

2 The Evolu tionary Process and the Fossil Record

Thermal overheating of marine faunas is negated as an explanation by the lack of terrestrial extinction (since vertebrates would be influenced before mar­ ine taxa), the prevalence of evaporites during the Kungurian and Middle Triassic (when no mass ex­ tinctions occurred), and the ability of most taxa to migrate to cooler (more polar) regions (Stanley in Nitecki 1984) . Stanley (in Nitecki 1984) suggested a global cooling, rather than glaciation-associated polar cooling at the close of the Permian, as a proximal cause of the extinction . He also argued that the effects of global cooling would be especially severe when preceded by a period of mild climate and equability - yet the Permian was a time of climatic instability . Despite the climatic oscillations there is no evidence for widespread Late Permian glaciation or a global cooling event, and maximum glaciation occurred in the Asselian - Sakmarian without a mass extinction . Marine productivity is highly dependent on nutri­ ents derived from land, particularly those delivered through estuarine ecosystems . Tappan (in Silver & Schultz 1982) suggested that the gradual decline in marine phytoplankton, zooplankton, and many filter feeders (corals, articulate brachiopods, stalked echinoderms, bryozoans) resulted from sequester­ ing of nutrients on land (as new plant communities developed) and in coal beds . Yet the groups most at risk diversified in the Lower Permian when the floral transition began, and coal beds (and maximum nutrient sequestering) predominated during the Carboniferous and Lower Permian . Declining mar­ ine productivity may well have played a role in the extinction, but if so the cause was unrelated to nutrient sequestering by land plants . The marine regression a t the close o f the Permian has been the most frequently cited ultimate cause of the extinction, but a causal connection to the extinc­ tions is unclear . Sea-level declined steadily through­ out the Permian, with a drop of about 210 m in the Dzulfian - Changhsingian to a point only 40 m below present day sea-level (Hallam 1984) . This left about 13% of the continental shelves covered. Short-term regressions of equal or greater magnitude occurred in the Upper Miocene, the Middle Oligocene, Lower Cretaceous, and Middle Triassic without associated mass extinctions, but began from higher sea stands, leaving more continental shelf area exposed than in the Permian . The cause of the Permian regression is unclear, but the most probable explanation is a cessation in mid-ocean ridge spreading as Pangaea formed, subsequent sinking of the ridges, and expansion of the volume of the ocean basins.

Logarithmic plots of species number versus area are frequently linear, giving the relationship : S kAz, where S is the number of species, A is total area, z is the slope of the regression of the log - log plot, and k is a constant . This empirically derived relationship, or species- area effect, implies that a regression will increase competition and thus extinctions . The species- area effect has been criti­ cized for a variety of ecological and palaeontological reasons but only a few are important here . Stanley (in Nitecki 1984) noted that since an island approxi­ mates to a cone in shape, the amount of habitable area increases during a regression . Jablonski (1986) calculated that 87% of the 276 families of molluscs, echinoderms and coelenterates that he analysed are present on one or more of the 22 oceanic islands studied . Consequently most marine families will be protected from the effects of a regression by occur­ rence on islands which expand in size . Perhaps of greatest importance, diversity does not seem to correlate well with available shelf area . For in­ stance the Hawaiian Islands contain approximately 1000 molluscan species while the tropical Pacific­ Panamic province, without the diverse coral reefs, contains about 3000 such species . Both regions have very small shelf area, and correspond well to the narrow, linear provinces which existed during the latest Permian . This suggests that high diversity faunas can exist in small regions and the species ­ area effect may b e spurious (Stanley i n Nitecki =

1984) . Marine provinces result from oceanic current pat­ terns and differing temperature optima among taxa . At least 12 Middle Permian marine faunal provinces can be confidently identified and additional work in Asia and South America should increase this number; many of these provinces, particularly in the Tethyan region, had very high species diversity . However earliest Triassic faunas are composed of cosmopolitan ammonoids, bivalves, inarticulate brachiopods, and chondrostean fish with low species diversity but high abundance . Yin (1985) identified six lowest Triassic bivalve provinces, while others have suggested a maximum of three provinces . Valentine & Moores (in Logan & Hills 1973; see also Schopf 1979) argued that the formation of Pangaea eliminated most marine provinces and played an important role in the extinction . The low Early Triassic provinciality and the cosmopolitan faunas may be a consequence of the extinction rather than a cause, however . The major continental suturing occurred in the Lower and Middle Permian, yet provinciality apparently re-

2 . 13 Mass Extinction: Events mained high until the end of the period . The declin­ ing provinciality is unlikely to be a consequence of the regression, since regressions restrict the areal extent of marine provinces but only reduce the total number if extensive epeiric seas are present, which was not true in the Late Permian . The large number of 'Lazarus-taxa' demonstrates that many taxa per­ sisted in as yet unidentified refugia. Marine regressions have important collateral side­ effects which may be the effective cause of extinc­ tion, including a loss of habitats, climatic changes and resulting resource instability, reduction or loss of facies-controlled community assemblages, and destruction of estuaries (a primary source of nutri­ ents) . Carbonate biomes are heavily affected at the end-Permian, and it may not be fortuitous that the Permian brachiopods found in the Tethyan mixed faunas are derived from underlying siliceous-facies assemblages . Marine regression also changes the Earth's al­ bedo, increasing continentality . As noted above, increasing continentality produces severe storms, high seasonality and exaggerated climatic fluctu­ ations (Valentine & Moores in Logan & Hills 1973; Jablonski 1986) . While many of these effects are terrestrial, increased seasonality will increase habi­ tat disturbance, particularly in tropical regions . Dur­ ing such periods generalists, which utilize a broad range of resources, and disturbance-tolerant, eury­ topic taxa will be favoured . Communities with large numbers of trophic specialists, typical of tropical areas, are highly efficient during periods of trophic stability but may be eliminated during unstable periods . Non-planktotrophic developers increase reproductive success by producing a few well adapted offspring and predominate in high lati­ tudes and seasonal environments . Valentine & Jablonski (see Valentine 1986) recorded the preferen­ tial loss of planktotrophic taxa in crinoids, articulate brachiopods, and archaeogastropods . This may have been due to the more speciose nature of non­ planktotrophic clades, or the increased trophic insta­ bility may have selected for non-planktotrophic developers . The high-latitude faunas where non­ planktotrophs predominate are dominated by trophic generalists . The most likely cause of the end-Permian mass extinction was tectonically-induced climatic insta­ bility and marine regression which brought about increased trophic instability (see Erwin 1990) . Independently none of these would have produced an extinction of this magnitude, but their simul­ taneous occurrence produced a synergistic reaction,

193

magnifying the result (this pattern corresponds well with those seen in non-linear dynamics) . The extinction of many marine plankton, sessile filter feeders, and high-level carnivores, and the relative success of disturbance-tolerant taxa, par­ ticularly in high latitudes, emphasizes the role of trophic instability . This occurred as seasonality and habitat destruction increased. Highly specialized communities were most affected, leaving broadly dispersed trophic generalists to populate the earliest Triassic . The end-Permian extinction also begins the 26.4 million year cycle of mass extinctions (Section 2 . 12.3) postulated by Raup & Sepkoski (the cycle may extend into the Palaeozoic, but the data are not sufficiently resolved at present) . This implies a causal connection between the end-Permian and end-Cretaceous extinctions (the two largest of the series) which should produce similar extinction pat­ terns . In fact, the two differ strongly. No iridium anomaly is present and the extinction patterns contrast sharply between the two events . The end­ Permian event shows no marked vertebrate extinc­ tions, unlike the extensive vertebrate extinctions of the Cretaceous (Section 2 . 13.7), and present evi­ dence suggests that the end-Permian extinction was of significant duration . The selective removal of marine invertebrates with a planktotrophic develop­ mental stage (crinoids, articulate brachiopods, and perhaps archaeogastropods) contrasts with the end­ Cretaceous when larval developmental mode had no effect on survival . The extensive evidence for tectonically-induced climatic change and trophic in­ stability in the Late Permian casts doubt on any causal link to the extinctions at the end of the Cretaceous .

References Clark, D . J . , Wang, C-Y . , Orth, c.J. & Gilmore, J . 5 . 1986. Conodont survival and low iridium abundances across the Permian-Triassic boundary in south China. Science 233, 984-986 . Erwin, D.H. 1990 . The end-Permian mass extinction. Annual Review of Ecology and Systematics 21, 69 -91 . Hallam, A. 1984. Pre-Quaternary sea-level changes. Annual Review of Earth and Planetary Sciences 12, 205 - 243 . Harland, W.B . , Cox, A.V., Llewellyn, P . G . , Pickton, C . A . G . , Smith, A . G . & Waiters, R. 1982 . A geologic time scale. Cambridge University Press, Cambridge. Jablonski, D. 1986. Causes and consequences of mass ex­ tinctions: a comparative approach. In: D.K. Elliot (ed . ) Dynamics of extinction, pp . 183-229 . John Wiley & Sons, New York. Knoll, A.H. 1984. Patterns in the fossil record of gasvascular plants. In: M.H. Iteki (ed . ) Extinctions, pp. 21 - 68 . Lin, J-L . , Fuller, M. & Zhang, W-Y . 1985 . Preliminary Pha-

2 The Evolutionary Process and the Fossil Record

194

nerozoic polar wander paths for the north and south China blocks. Nature 313, 444-449 . Logan, A. & Hills, LV. (eds) 1973 . The Permian and Triassic systems and their mutual boundary. Memoir of the Canadian Society of Petroleum Geologists, No. 2 . Nitecki, M . B . (ed . ) 1984 . Extinctions . University o f Chicago Press, Chicago . Schopf, T.J.M. 1979 . The role of biogeographic provinces in regulating marine faunal diversity through geologic time . In: J. Gray & A.J. Boucot (eds) Historical biogeography, plate tectonics and the changing environment, pp. 449 -457. Oregon State University Press, Corvallis. Sepkoski, J.L Jr. 1982. A compendium of marine families . Milwaukee Public Museum Contributions to Biology and Geology, No. 5I . Sepkoski, J .L Jr. 1986. Global bioevents and the question of periodicity. In: O. Walliser (ed . ) Global bio-events . Springer-Verlag, Berlin . Sheng, J . Z . , Chen, C . Z . , Wang, Y . G . , Rui, L , Liao, Z.T., Bando, Y . , Ishii, K . , Nakazawa, K . & Nakamura, K. 1984. Permian-Triassic boundary in Middle and Eastern Tethys. Journal of the Faculty of Sciences, Hokkaido Univer­ sity, Series IV 21, 133 - 18 1 . Silver, LT. & Schultz, P.B. (eds) 1982. Geological implications of impacts of large asteroids and comets on the Earth. Special Paper of the Geological Society of America No. 190 . Valentine, J.W. 1986 . The Permian-Triassic extinction event and invertebrate developmental modes . Bulletin of Marine Science 39 607-615. Xu, D-Y . , Ma, S-L , Chai, Z-F . , Mao, X-Y . , Sun, Y-Y . , Zhang, Q-W . & Yang, Z-Z . 1985 . Abundance variation of iridium and trace elements at the Permian-Triassic boundary at Shangsi in China. Nature 314, 154- 156 . Yin, H.F. 1985 . Bivalves near the Permian -Triassic boundary in south China . Journal of Paleont% gy 59, 572-600 . ,

2 . 13 . 5 End-Triassic M . J . BENTON

Introduction A mass extinction event in the Late Triassic has been recognized for some time . The decline and virtual disappearance of the ammonoids at the Triassic -Jurassic boundary has long been clear to cephalopod workers, while in the nineteen-forties Edwin Colbert described the major extinctions of terrestrial tetrapods at that time . Recent surveys of mass extinction events in the sea (e . g . Raup & Sepkoski 1982) have identified

the end-Triassic event as one of the five major Phanerozoic extinctions, equal in magnitude over­ all to the end-Ordovician (Section 2 . 13.2), Late Devonian (Section 2 . 13 . 3), and end-Cretaceous (Sections 2. 13.6, 2 . 13 . 7) events, with a loss of over 20% of approximately 300 families of marine inver­ tebrates and vertebrates . It is also one of the key extinctions in considerations of periodicity (Raup & Sepkoski 1984; Section 2. 12.3), occurring as it does about 26-30 million years after the end-Permian event.

Extinction patterns In the sea, several major lineages of invertebrates and vertebrates went extinct . The main groups to be affected were the cephalopods (58 families became extinct), the gastropods (13), various marine reptiles (13), the brachiopods (12), the bivalves (8), and the sponges (8) . The effects on the ceratitid cephalo­ pods, which were abundant and widespread in the Triassic, were dramatic - all 46 Late Triassic families died out - and the ammonoids as a whole barely survived into the Jurassic . When genera are considered, the Ceratitida reached a peak of c. 150 genera in the Carnian, which fell to c. 100 in the Norian, and to single figures in the latest Norian, finally disappearing at the Triassic -Jurassic bound­ ary . This corresponds to an extinction rate of 100% at all levels. Only the Phylloceratina passed, at very low diversity, from the Triassic into the Jurassic. The family extinction rate for bivalves was not so marked, but the generic extinction rate was 42%, and the species extinction rate, in Europe at least, was 92% (Hallam 1981) . This suggests that both the cephalopods and the bivalves barely scraped through the end-Triassic event into the Jurassic to establish new radiations . The last strophomenid brachiopods, conodonts, conulariids, nothosaurs, and placodonts also disappeared in the Late Triassic. On land, major extinctions occurred amongst the insects (35 families), the freshwater bony fishes (8), and the thecodontians (8) . There was a major faunal turnover amongst non-marine tetrapods in the Late Triassic, during which the formerly dominant laby­ rinthodonts, mammal-like reptiles, thecodontians, procolophonids, prolacertiforms, and rhynchosaurs died out, or were greatly depleted, and new groups, such as the dinosaurs, crocodiles, pterosaurs, turtles, lepidosaurs (lizards and their relatives), lissamphib­ ians (frogs and salamanders), and mammals came on the scene (Benton 1986; Benton; Olson & Sues in Padian 1986) .

195

2 . 13 Mass Extinction: Events


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Terrestrial events: competition or mass extinction? There was a global faunal turnover amongst ver­ tebrates on land in the Late Triassic . In several early papers, E . Colbert drew attention to the loss of a whole range of groups, as noted above . The nature of this massive replacement has been controversial . Initially, Colbert argued that the new groups radi­ ated into effectively empty ecospace after a series of extinctions . Thus, the new lizard-like animals occupied the niches that procolophonids and pro­ lacertiforms had held before, crocodiles filled the niches of the recently-extinct phytosaurs, and so on . However, views changed during the nineteen­ sixties and seventies to focus more on competition­ based models for the faunal replacement . The idea was that the dinosaurs outcompeted the formerly dominant mammal-like reptiles, rhynchosaurs, and thecodontians . The dinosaurs were said to have advantages in their style of locomotion (upright, instead of sprawling) and/or their thermal physi­ ology . Thus, some authors argued that the dinosaurs must have been fully warm-blooded (endothermic) in order to compete successfully, while others stressed the advantages of cold-bloodedness (the need for less food and water) . However, recent detailed analyses of the fossil data (reviewed in Benton; Olsen & Sues in Padian 1986) suggest that the long-term competitive models are not likely . The relative abundances of the maj or terrestrial tetrapod groups throughout the Triassic show that there was no gradual long-term decline of the earlier groups, and matching radiation of the replacing groups . The dinosaurs were in existence near the beginning of the Late Triassic (in the Carnian), but they were very rare elements in their faunas (1% or less of all individuals) (Fig. 1). Many ecologically important groups then disappeared at the end of the Carnian, as far as the data indicate (rhynchosaurs, various mammal-like reptiles, and thecodontians), and the dinosaurs radiated there­ after in the Early Norian . Further groups of theco­ dontians and mammal-like reptiles disappeared at the end of the Triassic, and the dinosaurs apparently radiated again . Other taxonomic studies on the diversity of tetra­ pod families in the Triassic (Benton 1986; Benton; Olson & Sues in Padian 1986) confirm the importance of mass extinction as the triggering factor for the remarkable faunal replacements in the Late Triassic . Indeed, there seems to have been more than one extinction event in the Late Triassic .

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Timing of the extinction events Was there one mass extinction event in the Late Triassic or several? Many studies (e . g . Raup & Sepkoski 1982, 1984) identify a single event, but a great deal of evidence now appears to disagree with that view . Several authors had already noted that the extinctions in the Late Triassic were either not synchronous in the sea and on land (e . g . Hallam 1981), or that the extinction lasted for much of the Late Triassic, through the Carnian and Norian (the latter including the 'Rhaetian'), a time-span of 1825 million years (depending on the time-scale used) . The timing of the Late Triassic marine extinction event has not been determined precisely for all groups . The bivalves declined in diversity from a Carnian - Early Norian peak, and were affected by a major extinction event at the end of the Norian (Hallam 1981) . Similarly, the ceratite ammonoids reached their peak of diversity in the Carnian, and declined thereafter . The last genera disappeared at the end of the Norian ('Rhaetian' ) . The mass extinc­ tions of brachiopods and conodonts appear to have occurred at the end of the Norian, while Benton (in Padian 1986); Olson & Sues (in Padian 1986) identified two extinction events for non-marine tetrapods, one at the end of the Carnian, and another at the end of the Norian .

196

2 The Evolutionary Process and the Fossil Record

The timing of the extinction of the marine ver­ tebrates has been disputed . It has generally been assumed (e .g. Raup & Sepkoski 1982) to coincide with the end-Triassic invertebrate extinctions . However, most of the Late Triassic marine reptile families died out in the Camian (five families), the timing of one is uncertain, and only one died out at the Triassic -Jurassic boundary: Benton (1986) presented three separate analyses that indicate at least two mass extinction events in the Late Triassic, one probably at the end of the Carnian, and the other 12- 1 7 million years later, at the Triassic -Jurassic boundary : 1 A detailed analysis of ammonoid families sug­ gests that there were several declines in family diversity, the largest two in the Camian and Late Norian (Fig . 2A) . Total extinction rates for am­ monoid families vary considerably during the Triassic and Early Jurassic (Fig . 2B), showing high peaks in the Late Scythian, the Late Ladinian, and the Early Camian, and smaller peaks in the Anisian and in the Middle and Late Norian . Per-taxon ex­ tinction rates (Fig . 2C) show high peaks in the Late Scythian, the Late Anisian, the Early Carnian, and the Late Norian . The Late Triassic 'mass extinction' of ammonoid families was not a single event, but at least two - one in the Camian, and a larger one at the end of the Norian (the 'Rhaetian') . 2 Triassic and Early Jurassic families o f non-marine tetrapods (Fig . 3A) show declines in diversity in the Early and Late Scythian, at the end of the Camian, and at the end of the Norian . These declines are matched by peaks in total extinction rate (Fig . 3B) and in per-taxon extinction rate (Fig . 3C) . The end­ Carnian mass extinction of non-marine tetrapods was apparently the larger of the two Late Triassic events, according to Benton (1986), while the analy­ sis by Olsen & Sues (in Padian 1986) suggested that the end-Norian event was larger than the end­ Camian one . These differences arise from the use of slightly different data sets . 3 Diversity and extinction rate data for all marine and non-marine animals in the Late Triassic (Benton 1986) indicate average marine diversity of about 340 families, and non-marine diversity of about 190 families . The numbers of family extinctions in mar­ ine taxa per time unit ranged from 3 to 54 (mean: 23 . 0), and in non-marine taxa from 4 to 45 (mean: 1 8 . 1 ) . The plots of marine and non-marine family diversity (Fig. 4A) showed declines at the end of the Camian, and smaller ones at the Triassic-Jurassic boundary . In all cases, both the total extinction rates (Fig . 4B), and the per-taxon extinction rates

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end-Permian t o end-Scythian: 5 - 6 Myr end-Scythian to end-Camian: 15- 19 Myr end-Carnian to end-Norian: 12-17 Myr If the periodicity theory of mass extinctions (Raup & Sepkoski 1984) is to be valid (Section 2 . 12.3), there should have been a single event 26- 30 million years after the end-Permian event, thus 219-222 Ma, in the Early Norian, according to current time­ scales. Present evidence on the Late Triassic record of marine and non-marine animals strongly contra­ dicts this prediction .

Causes The Late Triassic tetrapod extinctions have been linked to an increasing aridity observed in reptile­ bearing beds in various parts of the world (Benton in Padian 1986) . Associated with these climatic changes were abrupt floral replacements in the Norian. The Dicroidium flora of Gondwanaland was replaced by a world-wide conifer-bennettitalean flora at the end of the Norian ('Rhaetian') and in the Early Jurassic. It has been suggested that these

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Late Triassic and earliest Jurassic plant and animal families . A, Total diversity. B, Total extinction rates . C, Per­ taxon extinction rates. The data are plotted separately for marine (closed circles), non-marine (open circles), and total (open squares) families . The two mass extinctions (end­ Carnian; end-Norian) are indicated with arrows . The data were calculated by stratigraphic stage, except for the Norian which was subdivided into Lower, Middle, and Upper substages. Each Norian substage was assumed to have the same duration. For abbreviations see the legend to Fig. 2 . (After Benton 1986, b y permission from Macmillan Magazines Ltd . ) Fig. 4

climatic and floral changes could have led to the extinction of various tetrapod groups . Another view links the extinctions with marine regressions and

2 The Evolutionary Process and the Fossil Record

198

reduced orogenic activity . These would have re­ sulted in lower habitat diversity on land as new lowlands appeared, removal of reproductive bar­ riers, and lower speciation rates. Indeed, much of the decline in diversity of tetrapods at this time is linked to depressed origination rates . Several kinds of explanations have also been given for extinctions in the marine realm: widespread marine regression followed by an anoxic event (Hallam 1981; see also Section 2 . 12. 1), temperature changes, or extraterrestrial impact (Section 2 . 12.2) . Indeed, the last proposal is supported by the Manicougan crater in Canada (70 km in diameter) which is dated at 206-213 Ma. However, to date, no iridium anomaly or shocked quartz occurrence has been reported that coincides with either of the possible Late Triassic extinction events .

References Benton, M.J. 1986 . More than one event in the late Triassic mass extinction. Nature 321, 857� 861 . Benton, M.J. 1988 . The origins of the dinosaurs . Modern Geology 13, 14�56. Hallam, A. 1981 . The end-Triassic bivalve extinction event.

Palaeogeography,

Palaeoclimatology,

Palaeoecology

35,

1 � 44 . Padian, K. (ed . ) 1986. The beginning of the age of dinosaurs . Cambridge University Press, New York. Raup, D . M . & Sepkoski, J . J . , Jr. 1982 . Mass extinctions in the marine fossil record . Science 215, 1501 � 1503 . Raup, D . M . & Sepkoski, J . J . , Jr. 1984. Periodicity of extinctions in the geologic past. Proceedings of the National Academy of Sciences 81, 801 � 805 .

2 . 1 3 . 6 Cretaceous - Tertiary (Marine) F . SURLYK

between the Maastrichtian and Danian Stages . The Danian was, however, originally considered the end-Cretaceous Stage . Discussions about the stratigraphic position of the Danian first started with Bramlette & Martini's (1964) observation that a major turnover of calcareous marine plankton took place at the Maastrichtian - Danian boundary . The broad pat­ tern of marine extinctions is now known for both microfauna and flora, and macrofauna (see reviews by Kauffman 1984; Stanley 1987) . The detailed ex­ tinction pattern, however, is known only for planktic foraminifera and calcareous nannoplankton, al­ though new data are continually appearing for other microfossil groups. High-resolution strati­ graphic information on the extinction across the boundary is virtually non-existent for marine inver­ tebrates . Only a few groups have been studied and lend themselves to investigation on the basis of closely spaced sample series . While the broad extinction patterns at the stage level can be relatively easily assessed on the basis of the literature, all discussions on the detailed patterns across the boundary come down to the question of sampling . It is well known that sampling effects can modify diversity patterns on both regional and local scales . Signor & Lipps (1982) particularly empha­ sized the effect of reduced sample size and artificial range truncation in the top Maastrichtian . Although this may seem trivial, it is overlooked in most reviews of the end-Maastrichtian extinction . Oceanic micro- and nannoplankton have a more complete record because the sediment itself is com­ monly composed of their skeletal remains . This is particularly true of biogenic sediments deposited above the carbonate compensation depth . Data based on randomly collected macroinvertebrate fos­ sils, however, are poorly suited to illuminate the detailed nature of the extinction, and the existing data-base for invertebrates is totally inadequate to illustrate the short term nature and rate of extinction and diversification across the boundary .

A standard boundary sequence Introduction The alleged mass extinction at the end of the Meso­ zoic Era has been one of the most intensively de­ bated subjects within geology and palaeontology (see also sections 2 . 12.1, 2 . 12.2) . In the forefront of the discussion has been the meteorite impact hypo­ thesi s (see Alvarez et al . 1984) . The Mesozoic­ Cenozoic Era boundary is placed at the boundary

A maj or breakthrough in high-resolution strati­ graphy across the boundary was reached with the recognition that the same lithological and faunal succession could be traced over all major ocean basins (Smit & Romein 1985) . This 'standard K - T boundary event sequence' contains a succession of five lithological units (1 - 5) which reflect the se­ quence of events across the boundary . The sequence

2 . 1 3 Mass Extinction: Events (or parts of it) was recognized in almost every boundary section world-wide . Unit 1 represents the uppermost Cretaceous and usually consists of pel­ agic calcareous oozes, limestones or marls . Unit 5 is in almost all respects comparable to unit 1 except for the completely new planktic biota of the Palaeocene . The thickness of the transitional interval between the Cretaceous and the Tertiary periods represented by units 2-4 amounts to no more than a few tens of centimetres in most sections. An exception is El Kef in Tunisia which shows the most complete evo­ lutionary development of planktic foraminifera at the base of the Palaeocene . Here the transitional interval is almost 2 m thick . The analysis of Smit & Romein (1985) showed that the shift from dominant­ ly Cretaceous to dominantly Palaeocene forms is consistently later for the nannoplankton than for the planktic foraminifera . The latter disappear within centimetres above the boundary, the former 10-50 cm higher in the section . This raises a very important question concerning the precise defi­ nition of the boundary . Should it be drawn at the mass extinction level, the iridium level (these two levels may coincide), the level of extinction of the last Cretaceous species, or at the first appearance of true Palaeocene taxa? This question still remains to be settled and it requires further detailed work on selected sections. Smit & Romein (1985) suggested that the standard K-T sequence could serve as a reference for all K - T boundary sections . It was interpreted as caused by a major impact, followed by a series of longer lasting biotic stresses . This interpretation can probably not be fully upheld, as will be shown below.

Microp lankton Work on the planktic foraminifera of the El Kef section by Keller (1988) demonstrated that the species extinctions prior to the assumed impact event cannot be explained by such a single impact, but suggest that multiple causes may be respon­ sible . Keller' s detailed study of the boundary at El Kef (Fig . lA, B) revealed that the mass extinction of planktic and benthic foraminifera occurred over an extended period beginning well before and ending after the boundary . In contrast, geochemical data indicate a geologically instantaneous event at the boundary . The expanded sediment record at El Kef shows that the boundary extinctions of planktic foraminifera extend over an interval from 25 cm below the geochemical boundary (iridium anomaly) to 7 cm above .

199

Species extinctions appear sequential with com­ plex, large, ornate forms disappearing first and smaller, less ornate forms surviving longer. Cre­ taceous species survivorship is greater than previously thought . Twenty-two percent (ten species) survive into the third subzone (Globigerina eugubina) . The survivors are small primitive forms which are generally smaller than their ancestors . Species evolution after the boundary event occurred in two pulses . The first new Palaeocene species are found in the basal black clay immediately after the major Cretaceous extinctions . These evolving species, which define the first two subzones, are small and primitive, similar to the survivor species . The second pulse in species evolution occurred in the lower part of the third subzone and is charac­ terized by larger, more diverse species . The first major increase in carbonate productivity occurred at this time, reflecting the recovery of the ecosystem nearly 300 000 years after the boundary event. The boundary extinctions largely affected deeper­ dwelling planktic species, and surface dwellers survived longest. Keller concluded that the species extinctions prior to the generally assumed impact event (implied by the iridium anomaly), and the long recovery period of the ecosystem thereafter, cannot be explained by a simple impact . Multiple causes may be responsible, such as climatic changes, a sea-level drop, production of warm saline bottom water, and the chemical consequences associated with increased salinity . Benthic foraminifera were, on the other hand, much less affected by the boundary crisis . However, Keller recorded a 50% reduction in species diversity at the boundary at El Kef, and the diversity remained 37% lower during deposition of the first 3 m of Danian sediments . The surviving species were gen­ erally tolerant of low O2 conditions and productivity was low . Keller worked with very densely spaced sample series and, even more importantly, also analysed smaller sample size fractions (63 - 150 !-lm) than the normal > 150 !-lm . This procedure fundamentally changed earlier concepts of the detailed nature of the microplankton boundary extinctions . All species in the earliest Tertiary assemblages are smaller than 150 !-lm, leaving Cretaceous survivors, as well as the rapidly evolving earliest Tertiary forms, unrecorded in the normally studied fraction . N annoplankton

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Fig. 1 A, Species ranges of planktic foraminifera at El Kef, Tunisia. Species extinctions begin 25 cm below the Maastrichtian­ Danian boundary and continue to 7 cm above the boundary. Ten Maastrichtian species survive into the Danian (thin lines) . Scattered occurrences of probable reworked Maastrichtian species omitted. (After KeIler 1988 . ) B, Cretaceous survivors and post­ boundary evolution for planktic foraminifera, CaC03 and stable isotope data across the Maastrichtian- Danian boundary at El Kef, Tunisia . (Modified from KeIler, G. & Lindinger, M . , unpublished observations . ) C, Brachiopod species range chart for the Middle Coniacian- Lower Danian chalk of northwest Europe . Note the striking contrast between Late Cretaceous background extinction and the mass extinction and adaptive radiation at the Maastrichtian- Danian boundary. (After Johansen 1988 . D, Brachiopod species ranges at Nye Kiov, Denmark. (After SurIyk & Johansen 1984, by permission of the AAAS; Johansen 1987. )

2 . 13 Mass Extinction: Events detail across the boundary . The Coccolithophorida were once thought to go virtually extinct at the boundary . Cretaceous species are common in the basal Tertiary strata but were until recently always described as reworked forms . By ingenious isotope work, however, Perch-Nielsen et al. (1982) suc­ ceeded in demonstrating that the Cretaceous nannofossils in the lowest Tertiary sediments actually survived the boundary . These relic species became extinct some tens of thousands of years after the actual boundary, probably as a conse­ quence of the environmental stress following the boundary events . The latest Cretaceous and the earliest Tertiary oceans contained significantly dif­ ferent isotopic signals, which were incorporated into the tests of the calcareous nannofossils . How­ ever, the Cretaceous species which dominate (to nearly 100%) the very lowermost Tertiary sediments have isotopic values different from those below the boundary . Perch-Nielsen et al . (1982) accordingly suggested that, in order to carry an Early Tertiary isotope signal, the nannofossils must have lived in the Early Tertiary oceans. That is, most of the typically Cretaceous species actually survived the mass extinction associated with the boundary . Survivors are most common in the basal Danian of high- and mid-latitude sites, whereas they are rare and only occur sporadically in low latitudes . The earliest Danian assemblages are of low diversity and short-term blooms of so-called disaster forms Thoracosphaera and Braarudosphaera are characteristic. Other groups of marine microplankton have not received the same detailed study . Dinoflagellates were evidently much less affected by the boundary events, but an unusually high rate of species turn­ over across the boundary has been recorded in Danish localities by J.M. Hansen . A number of characteristic Maastrichtian species disappear at the top of the Maastrichtian while a succession of new Tertiary species rapidly appear in the lowermost Danian . The concentration of dinoflagellates in the boundary clay is extremely high, possibly rep­ resenting blooms . Diversity is also high and there is a dearth of opportunistic species; this indicates non-stress conditions for this microplankton group .

Inverte brates The problem of sampling effects becomes much more important for the record of marine inver­ tebrates . Few facies are sufficiently fossiliferous to allow dense sampling . Even more limiting is the

201

rarity of richly fossiliferous shallow-marine Upper Maastrichtian sections, not to speak of relatively complete boundary sections . The sections most commonly mentioned in the literature are those at Stevns Klint and Nye Khw in Denmark, and at Braggs and Brazos River in the U. S . A . The frequently cited Spanish localities around Zumaya show deep­ water sequences which are extremely poor in benthic invertebrate fossils, while ammonites are common and diverse in the Lower Maastrichtian part of the sections . Characteristic Cretaceous bivalve groups such as rudists and inoceramids experienced severe attrition before the end of the Cretaceous . Only about four inoceramid genera made their way into the Maastrichtian and no true inoceramid species are known from Upper Maastrichtian strata. The reef-forming rudists flourished in great diversity earlier in the Cretaceous, reaching a climax in the Late Campanian to Early Maastrichtian. They were decimated at the beginning of Late Maastrichtian time and were virtually extinct by the end of this stage . The problems of sampling and preservation are illustrated by Heinberg's (1979) study of the bivalves across the boundary at Stevns Klint. The topmost 3.5 m of the Maastrichtian is developed here as low mounds of bryozoan chalk (see Alvarez et al . 1984, fig . 1 ) . The mound summits are incorporated in a complex early (but not basal) Danian hardground . Early lithification predated aragonite dissolution and ensured the fortuitous mould preservation of minute aragonite shelled bivalves otherwise un­ known from the Maastrichtian chalk. The fossil record of most chalks is thus highly distorted by the artificial dominance of calcite shelled taxa; Heinberg's work gives a tantalizing glimpse of the complete bivalve fauna once present . His data (on genera only) show that 13 typically Tertiary genera first appear in the lithified top of the Maastrichtian . He therefore concluded that the terminal Cretaceous faunal turnover in bivalves was under way before the boundary, indicating a graded faunal transition . Twelve of these genera are dominantly aragonitic and the ranges of ten were substantially extended back in time when they were recognized in the hardground . They almost certainly represent older Cretaceous groups that survived the extinction event, rather than the sudden advanced appearance of Tertiary forms before the mass extinction . Of the ten genera last appearing in this hardground, four had partially calcitic shells and their apparent extinc­ tion at this level is probably real . It is very likely

202

2 The Evolutionary Process and the Fossil Record

that the extinction at species level was more dra­ matic, such as that seen in the brachiopods and to some extent also bryozoans . The fate of the chalk brachiopods has been studied in most Danish sections and a particularly detailed sample sequence has been described from the locality Nye Kiev (Fig . 10) . The uppermost Maastrichtian at Nye Kiev contains 27 species. Thirteen of these also occur in the 3 cm thick boundary clay; they have never been found higher in the Danian sequence, are broken, worn and non­ transparent, and were probably contained in smears of Maastrichtian chalk which are common in the clay. The possibility that they represent very short term survivors cannot, however, be excluded. Six species are common to the Maastrichtian and the Danian Stages and represent true survivors . They are long-ranging, morphologically un specialized forms which were probably environmentally toler­ ant generalist species . Finally, 23 species appear for the first time in the Danian 4-5 m above the boundary . The same picture is known, albeit in less detail, from other Danish boundary localities . The end­ Maastrichtian extinction seems to coincide with the base of the boundary clay, although several species last appear a few centimetres below the boundary . This may be taken to reflect their true extinction but is more likely a trivial sample effect (cf. Signor & Lipps 1982) . The species diversity curve shows no systematic decrease at the end of the Maastrichtian . Several workers have focused on the barren interval above the boundary clay and have suggested the possibility that some of the Maastrichtian species survived for a time, possibly in the same refuge as the six survivors . This is certainly very likely but, with only a few exceptions, species found at a later date in the 'barren' interval in Nye Kiev and in correlative deposits at other Danish localities belong to the six surviving generalist species . The extinction pattern noted for the brachiopods (Fig. 1C, D) was interpreted on purely ecological grounds . The fauna was specialized to the extensive macrohabitat of the chalk sea bottom and is virtually unknown outside this environment . Chalk pro­ ductivity essentially stopped at the end of the Maastrichtian as a result of the calcareous micro­ plankton crisis and extinction . The combined effects of the cessation of chalk production, the onset of clay deposition, hardground formation, and possibly low oxygenation at the sea floor caused the geo­ logically instantaneous destruction of a unique macrohabitat of great longevity . The immediate

result was the mass extinction of faunal groups specialized to the chalk substrate, such as the brachiopods described above . When chalk pro­ duction was eventually resumed in the Early Danian, adaptive radiation within surviving groups led to rapid restoration of the chalk macrohabitat and its fauna . Much attention has been focused on the ammon­ ites because they are a very characteristic Mesozoic faunal element which forms the basis for Mesozoic stratigraphy, and because they became extinct at the boundary . It is widely accepted that reduction in the diversity of ammonites had been in progress for several million years before the boundary . Genera and families fall into two groups . The first includes long-lived taxa, which neither increased nor decreased dramatically in diversity through time . The second group, composed of short-lived taxa, accounts for most of the variations in abun­ dance and diversity . Nine species representing seven genera and six families occur in the topmost Maastrichtian of Denmark . They belong to a wide range of highly different morphotypes, probably reflecting different modes of life . The extinction of these taxa was the critical and unpredictable event . Without it the ammonites would not have disap­ peared . The Zumaya locality contains a diverse Lower Maastrichtian ammonite fauna, but the diversity rapidly decreases and the topmost Maastrichtian contains only few ammonites . This has been taken possibly to reflect an earlier ex­ tinction in a tropical, Tethyan environment, as compared to the Boreal chalk sea, but this may be putting just too much weight on an extremely poorly fossiliferous interval in a section . For comparison, ammonites are extremely rare in the main part of the Lower Maastrichtian of Denmark while they occur in abundance in the uppermost Lower and Upper Maastrichtian . Our knowledge of the fate of marine vertebrates is very limited compared to that of the micro­ plankton and the main invertebrate groups . The mosasaur and plesiosaur reptiles became extinct some time during the Maastrichtian together with the largest marine turtles, but nothing is known concerning the timing of the extinction . The end-Cretaceous extinction is thus of a com­ plex nature and the scenario has been variously described as invoking a 'multiplicity of interacting factors', as 'multicausal' or as a 'compound crisis' . Taken alone such phrases are merely cliches which are difficult to test, and they should not

203

2 . 13 Mass Extinction : Events provide a let-out from undertaking a more precise interpretation of the available data .

2 . 13 . 7 Cretaceous - Tertiary (Terrestrial)

References Alvarez, W., Kauffman, E . G . , Surlyk, F., Alvarez, L . W . , Asaro, F. & Michel, M.V. 1984. Impact theory of mass extinction and the invertebrate fossil record . Science 223, 1 1 35 - 1 14l . Bramlette, M.N. & Martini, E. 1964 . The great change in cal­ careous nannoplankton fossils between the Maastrichtian and the Danian. Micropaleontology 10, 291 - 322. Heinberg, C . 1979 . Bivalves from the latest Maastrichtian of Stevns Klint and their stratigraphic affinities . In: T. Birkelund & R . G . Bromley (eds) Cretaceous-Teritary Boundary Events Symposium. I. The Maastrichtian and Danian of Denmark, pp. 58-64. University of Copenhagen, Copenhagen. Johansen, M.B. 1987. Brachiopods from the Maastrichtian­ Danian boundary sequence at Nye Klov, Jylland, Denmark. Fossils and Strata 20, 1 -99 . Johansen, M . B . 1988 . Brachiopod extinctions in the Upper Cretaceous to lowermost Tertiary chalk of northwest Europe . In: Paleontology and evolution, pp . 41 - 56 . Revista Espanola de Paleontologia, no . Extraordinario 1988 . Kauffman, E . G . 1984. The fabric of Cretaceous marine extinc­ tions . In: W.S. Berggren & J . A . van Couvering (eds) Catastrophes and Earth history: the new uniformitarianism, pp . 151 -246 Princeton University Press, Princeton. Keller, G. 1988. Extinction, survivorship and evolution of planktonic foraminifera across the Cretaceousrrertiary boundary at El Kef, Tunisia. Marine Micropaleontology 13, 239 - 263 . Perch-Nielsen, K., McKenzie, J. & He, Q. 1982. Biostratigraphy and isotope stratigraphy and the 'catastrophic' extinction of calcareous nannoplankton at the Cretaceousrrertiary boundary. Special Paper of the Geological Society of America 190, 353-371 . Signor, P.W., III & Lipps, J . H . 1982 . Sampling bias, gradual extinction patterns and catastrophes in the fossil record. Special Paper of the Geological Society of America 190, 291 - 296. Smit, J . & Romein, A.J.T. 1985 . A Sequence of events across the Cretaceous- Tertiary boundary. Earth and Planetary Science Letters 74, 155 - 1 70. Stanley, S.M. 1987. Extinction . Scientific American Books, New York. Surlyk, F. & Johansen, M . B . 1984. End-Cretaceous brachiopod extinctions in the chalk of Denmark. Science 223, 1 174- 1 1 77 .

L . B . H A L S T E AD

Introduction The extinction of the dinosaurs is generally con­ sidered to be one of the most dramatic events in the Earth's history. The potential significance of the event was enormously enhanced by the suggestion by Alvarez et al . (1980) that the demise of dinosaurs could be attributed to the impact of a large Earth­ crossing asteroid (Section 2 . 12.2), indicated by iridium enrichment at the Cretaceous- Tertiary boundary. This publication sparked off a consider­ able debate which emphasized the di£fering meth­ odologies of physicists and palaeontologists (see analysis by Clemens 1986) . An alternative view (Section 2 . 1 2 . 1) is that it is not necessary to postulate the impact of an extra-terrestrial object to account for the iridium enrichment, but that volcanic activity provides a more reasonable explanation . This is supported by the accumulated evidence that the end-Cretaceous extinctions of different animal and plant groups on both land and in the seas were not synchronous (Section 2 . 13.6) . When attempting any discussion of the Cretaceous - Tertiary extinction on land, it is important to recognize that an un­ broken sedimentary transition of terrestrial sedi­ ments is only known in an area in Western Canada and the U . 5 . A . extending from Alberta in the north through Montana, Wyoming, and Colorado to New Mexico in the south .

Plants A study of the record of plants by Wolfe & Up­ church (1986) revealed a dramatic change at the Cretaceous - Tertiary boundary with a sharp peak of distribution of fern spores . This widespread fern spike is usually taken as a sign of wildfires . Once fire has swept through an area, the first plants to re colonize are usually ferns and their allies, and this event is picked up in the fossil record as a fern spike . Wildfires can be attributed to either volcanic activity or asteroid impact . It is perhaps significant that a similar fern spike was identified at the Cretaceous - Tertiary boundary in marine sediments from Hokkaido island, Japan, by Saito, et al. (1986),

2 The Evolutionary Process and the Fossil Record

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Mammals The record of terrestrial vertebrates has been care­ fully documented by Archibald & Clemens (1982; 1984) . Microvertebrates (mainly mammal teeth) have been carefully collected across the Cretaceous ­ Tertiary boundary . A clear pattern emerges of gradual change (Fig. 2). The multituberculates, with their chizel-like incisors, must have occupied the gnawing-nibbling niche, and continued into the Tertiary with relatively little change . The small herbivorous condylarthrans began a modest increase in both numbers and diversity, and by Early Tertiary times had become the major her­ bivores . By far the most significant change in the mammalian fauna was the drastic reduction in the number of species of marsupials, with basically

only the oppossum continuing through to the Tertiary . The primitive proteutherian insectivorous mammals seem to have declined in the Late Cre­ taceous and then recovered in the Tertiary, achiev­ ing a modest increase in diversity compared with the preceding Cretaceous . The pattern of mammalian distribution through time demonstrates a gradual replacement of more typical Cretaceous forms by Tertiary types . This gradual turnover began well before the Cretaceous ­ Tertiary boundary . There is clear evidence that sig­ nificant faunal changes occurred around the time of the Cretaceous - Tertiary boundary, but there was no sign of any dramatic event taking place at the boundary itself.

205

2 . 13 Mass Extinction: Events Reptiles The general consensus is that the dinosaurs all died out during the Cretaceous . It has been claimed, however, that seven dinosaur genera survived into the basal Tertiary. Dinosaur bones were discovered in channel deposits containing typical Palaeocene mammals (Sloan et al. 1986) . The claim has been disputed with some vigour (see Retallack & Leahy 1986 and discussion) . Whether or not the existence of Palaeocene dinosaurs is confirmed, what is clearly established is that from the Campanian (as seen in the Dinosaur Provincial Park, Alberta) through the Horseshoe Canyon Formation to the Hell Creek and Lance Formations the dinosaurs were beginning to go into a serious decline and that during the last 300 000 years of the Cretaceous this decline was greatly accelerated (Fig. 3) . Both numbers of specimens and diversity were drastically reduced . Van Valen & Sloan (1977) assembled evidence which suggested a gradual southwards migration of dinosaurs in the wake of an invasion by large numbers of herbivorous condylarthran mammals, and by more temperate plant life which replaced the humid broad-leaved evergreen forests . The distinct impression is left, however, that the end for the few remaining dinosaurs was sudden . It is therefore instructive to examine the record of reptiles across the Cretaceous - Tertiary boundary (Sullivan 1987) (Fig . 4) . Among the chelonians (turtles and tortoises) only the family Protostegidae died out at the end of the Campanian . Six other families crossed the boundary well into the Tertiary and ranged beyond the Palaeocene . The crocodile-like eosuchians (the Champsosauridae) ranged through the latter part of the Campanian, the Maastrichtian, and the Palaeocene . Three families of crocodile ranged through into the Tertiary . Several families of lizard similarly survived into the Tertiary with no evidence of any change : the agamids, anguinids (slow­ worms), the iguanas, teids, and varanids . A number of groups known from the Tertiary, however, are not certainly known from the uppermost Cretaceous, such as the Gila monster, the helodermatids, the necrosaurs, skinks, and the xenosaurids . Of the snakes only the boids (boas) spanned the entire Campanian through to the present . Thus the Cretaceous - Tertiary boundary was no barrier to chelonians, eosuchians, crocodiles, lizards, and snakes. When the record of the dinosaurs is examined in

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comparable detail it is strikingly evident that most genera became extinct before the Cretaceous ­ Tertiary boundary (Fig. 4) . The giant scavenging carnivores Tyrannosaurus and Albertosaurus reached the boundary; the lightly built clawed carnivorous dromaeosaurs are known from a few fragments at the boundary . The ornithomimids (ostrich dinosaurs) died out just prior to the boundary, and the last surviving sauropod Alamosaurus did not reach it . The primitive small ornithopod Thescelosaurus, a surviving hypsilophodont, reached the end of the Cretaceous . The primitive non-crested hadrosaur Edmontosaurus reached the boundary . One of the armoured dinosaurs Euplococephalus made it, whereas another genus Panoplosaurus became extinct at the base of the Lancian . Among the bone­ heads, the well known genera Stegoceros and Pachycephalosaurus had died out before the bound­ ary but one genus Stygimoloch managed to reach it. The only North American protoceratopsid Leptoceratops died out in the Edmontian and only two ceratopsians continued to the end : Triceratops reached the boundary, while Torosaurus did not quite make it.

206

2 The Evolutionary Process and the Fossil Record

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I t appears that only 12 species o f dinosaur reached the Cretaceous - Tertiary boundary. It becomes difficult to regard the end-Cretaceous event as a mass extinction of the terrestrial biota. The fossil record certainly documents important biological changes, but they indicate a serious decline in part of the fauna during the Late Cretaceous, with a significant acceleration of the process towards the boundary itself.

References Alvarez, L . W . , Alvarez, W . , Asaro, F. & Michel, H.V. 1980. Extraterrestrial cause for the Cretaceous -Tertiary extinc­ tion. Science 208, 1095 - 1 108. Archibald, J . D . & Clemens, W.A. 1982 . Late Cretaceous extinctions . American Scientist 70, 377 - 385. Archibald, J . D . & Clemens, W.A. 1984. Mammal evolution near the Cretaceous -Tertiary boundary . In: W . 5 . Berggren & J.A. van Couvering (eds) Catastropes and Earth history: the new uniformitarianism, pp. 339 - 371 . Princeton

University Press, Princeton . Clemens, E . S . 1986 . Of asteroids and dinosaurs: the role of the press in the shaping of scientific debate . Social Studies of Science 16, 421 - 456. Retallack, G . , Leahy, G . D . , & Sheehan, P.M. 1986 . Cretaceous - Tertiary dinosaur extinction. Science 234, 1170 - 1 1 71 .

Saito, T . , Yamanoi, T . & Kaiho, K . 1986 . End-Cretaceous devastation of terrestrial flora in the boreal Far East. Nature 323, 253- 255. Sloan, R . E . , Rigby, J.K., Van Valen, L.M. & Gabriel, D . 1986 . Gradual dinosaur extinction and simultaneous ungulate radiation in the Hell Creek Formation. Science 232, 629 - 633.

Sullivan, R.M. 1987. A reassessment of reptilian diversity across the Cretaceous -Tertiary boundary. Contributions in Science 391, 1 -26. Van Valen, L.M. & Sloan, R.E. 1977. Ecology and extinction of the dinosaurs . Evolutionary Theory 2, 37-64 . Wolfe, J.A. & Upchurch, G . R . 1986. Vegetation, climatic and floral changes at the Cretaceous - Tertiary boundary. Nature 324 , 148- 154.

207

2 . 13 Mass Extinction: Events

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2 . 1 3 . 8 Pleistocene E . L . LUNDELIUS , Jr

Introduction One of the major world-wide biological events of the last million years was the extinction of numerous taxa of mammals and a few lower vertebrates . This extinction event differed from those at the end of the Permian (Section 2 . 13 .4) and the Cretaceous (Sections 2 . 13 . 6, 2 . 13 . 7) in that it primarily affected large (i . e . more than 44 kg) terrestrial mammals, rather than the much greater variety of vertebrate and invertebrate animals from both marine and terrestrial habitats that characterized earlier extinctions .

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Extinction patterns In North America, 33 genera of large and four genera of small (i . e . less than 44 kg) mammals disappeared . South America lost up to 46 genera of large mam­ mals . In Europe, of 13 genera that disappeared, only three became totally extinct while others survived elsewhere (Martin in Martin & Klein 1984) and there was no significant loss of small animals . Data from Africa and Asia are too sparse to give a comprehen­ sive picture, but it appears that Southern Africa lost at least six species and Northern Asia lost about three . Fifteen genera (48 species) of mammals, three large reptiles and one large bird became extinct in Australia. Many of the North American species that became extinct, such as several ground sloths (Glossotherium, Eremotherium, Nothrotheriops, and Megalonyx), saber­ toothed cats (Smilodon, Homotherium), giant short­ faced bears (Arctodus), large peccaries (Platygonus, Mylohyus), glyptodonts (Glyptotherium), and giant

2 The Evolu tionary Process and the Fossil Record

208

Martin & Klein 1984) . The number of genera and species in other families, such as the Macropodidae and Vombatidae, were reduced. The exact time and duration of the extinction events were not the same on all continents . In North America an extensive list of radiocarbon dates indi­ cate that most of the extinctions occurred between 13 000 and 9000 years BP. A critical review of the youngest radiocarbon dates for 20 genera (Mead & Meltzer in Martin & Klein 1984) suggests that most of the taxa disappeared in a narrow time interval between 12 000 and 10 000 BP (Fig . 1 ) . In Europe the disappearance of the large mammals spanned a longer period of time, perhaps beginning as early as 20 000 BP and ending about 11 000 BP. In southern Africa the major extinction event took place between 12 000 and 9500 BP (Klein in Martin & Klein 1984) . In Australia the extinctions began about 25 000 BP and continued until 1 1 000 BP. The major effect of these extinctions was a great reduction in diversity of the large mammal component of the faunas of these continents . An examination of the pattern of extinction in North America in the last ten million years indicates that the terminal Pleistocene extinction was only the last in a series of extinctions that occurred at 9, 6, 5, 1 .9, and 0 . 5 Ma . For reasons that are not understood, the earlier extinctions exter­ minated a larger proportion of small animals than did the last one . Tentative correlations with the deep sea glacial/interglacial chronology indicate that the extinctions coincided with deglaciation events, particularly with those that ended longer and/or

armadillos (Holmesina) were the last representatives of formerly much more diverse genera and families . The extinction of the mastodon (Mammut) and the last two species of mammoths (Mammuthus jeffersoni and M. primigenius) terminated a whole order of mammals, the Proboscidea, in North America . The extinction of all these taxa resulted in the disappear­ ance of a large number of adaptive types . I n South America, the extinct taxa included the last representatives of the indigenous or­ ders Notoungulata and Liptopterna, which con­ tained one and two genera respectively . In the order Edentata four families, the Glyptodontidae (nine genera), and three families of sloths - the Megalonychidae (three genera), the Megatheriidae (two genera), and the Mylodontidae (five genera) disappeared . Two other groups of indigenous South American mammals, the armadillos, and the caviomorph rodents, suffered losses. Several groups of North American origin, such as the proboscideans and horses, disappeared completely, while others, such as the camels, felids, and cervids, underwent a loss of diversity. Eurasia and Africa had fewer losses . Most of the forms that disappeared in Europe survived in other continents, primarily Africa, and only one taxon, the saber-tooth cat Homotherium, represented a totally extinct adaptive type . There were few extinc­ tions in Africa during the Late Pleistocene and these were at the specific or generic level. In Australia, three families of marsupials Palorchestidae, Diprotodontidae, and the Thylacoleonidae - became extinct (Murray in

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2 . 1 3 Mass Extinction: Events more severe glacial stages (Webb in Martin & Klein 1984) . Causes

The two most commonly proposed hypotheses as to the causes of the terminal Pleistocene extinctions are human overpredation and the destabilization of habitats caused by climatic change . The model for human overpredation relies on the apparent coinci­ dence in time between the arrival of humans in North America and the disappearance of the large mammals (Martin in Martin & Klein 1984) . On other continents, where these migrations did not occur, it has been proposed that new, and presumably more sophisticated, hunting techniques were developed and contributed to the extinction of prey species (Klein in Martin & Klein 1984) . The case for the climatic hypothesis depends on a coincidence in time between the extinction event and the extensive environmental changes that

209

occurred at the end of the last glacial stage . A shift from an equable to a more seasonal climatic regime is indicated by the presence, within the same fossil deposits, of sympatric associations of extant species whose ranges have become markedly allopatric since 1 1 000 BP. Palynological data show a loss of similar associations of plant species at this time with a consequent depletion of niches resulting from a reduction in local plant diversity. The loss of these associations closely coincides with the extinc­ tions of the large mammals in all parts of the world for which there are adequate data (Lundelius 1983; Graham & Lundelius in Martin & Klein 1984) . References Lundelius, E . L . , Jr. 1983. Climate implications of late Pleistocene and Holocene faunal associations in Australia. Alcheringa 7, 125 - 149 . Martin, P.S. & Klein, R . C . (eds) 1984 . Quaternary extinctions: a prehistoric revolution . University of Arizona Press, Tucson .

3

TAPH O N O MY

courtesy of R . B . Rickards . )

Current aligned specimens of the Silurian graptolite

Monograptus riccartonensis, x 6 .

(Photograph

3 . 1 IJecay Processes P . A . ALLISON

Introduction

organic carbon using O 2 as the principal electron donor and produce CO2 and water as by-products . Following the depletion of O2 the microbes are forced to utilize a series of alternative electron ac­ ceptors (such as N0 3 -, Mn0 2 , Fe(OHh, and SO l -) for the respiration of organic carbon (see Section 3 . 8 . 2 for equations) . The ordering of these reactions is controlled by the free-energy yield of the reaction. Thus, in the ideal case, these reactions would be layered - with those liberating the greatest free­ energy nearest the sediment- water interface . Fol­ lowing the depletion of one of these oxidants, the sediment microbiota respire using the next most efficient reaction . When the oxidants have been fully depleted, degradation proceeds by fermen­ tation during which organic matter is broken down by enzymes and CO 2 is reduced to methane . How­ ever, not all these oxidants are present in any given environment; typically sulphate reduction and methanogenesis dominate in a marine system, while methanogenesis alone dominates in fresh­ water. There are therefore three common decay regimes in aquatic sediments : (1) aerobic (in marine and freshwater systems); (2) marine anaerobic (sulphate reduction and methanogenesis); and (3) freshwater anaerobic (principally methanogenic although nitrate reduction and iron reduction may be important in some systems) . Aerobic decay pro­ cesses are commonly considered the most rapid and effective means of biodegradation . Thus euxinic conditions are generally accepted as a prerequisite for the preservation of lightly skeletonized and soft­ bodied organisms . However, the oxygen require­ ment for aerobic decomposition is high . For instance, the decomposition of one mole of organic matter requires 106 moles of oxygen:

Decay processes are responsible for substantial pres­ ervational bias in the fossil record . The most obvious effect of this bias is the rarity with which organic soft parts are preserved. Such a bias has considerable importance for the palaeontologist since soft-bodied organisms may represent up to 60% of the indivi­ duals in a marine community (Jones 1969) . Where organic soft parts are encountered in the fossil record, they are indicative of exceptional sedi­ mentological and diagenetic conditions . It is im­ portant to note, however, that the preservation of soft parts does not necessarily imply a minimal preservational bias. At some localities the con­ ditions leading to soft part preservation have pro­ moted the dissolution of biogenic hard parts . A good example is provided by the Iron Age 'Bog­ people' of Northen Europe (Glob 1969) . These human cadavers include cellular detail of skin, muscle, hair and clothes preserved from decay by tannic and fulvic acids in the peat. However, these conditions also promoted the dissolution of bone . In the extreme case cadavers occur as a body-shaped bag of skin devoid of hard parts . Under normal conditions decay processes are initiated by death and continue until a carcass is either completely destroyed or mineralized. If min­ eralization occurs after a period of prolonged decay then the overall level of preservation will be low; if, on the other hand, mineralization occurs prior to appreciable decay then the level of preservation will be high . Process

Dead organisms are a valuable food source in any environment . If this food source is utilized by macro-organisms it is termed scavenging; if it is utilized by microbes, such as fungi and bacteria, it is termed decay . Rate of decay is controlled by three factors : (1) supply of oxygen and other electron donors; (2) environmental factors such as tempera­ ture, pH, and sedimentary geochemistry; and (3) the nature of organic carbon . In an aerated environment, microbes break down

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213

214

3 Taphonomy

as 335 cm3/g of carbon/half-life . With such a high oxygen requirement, demand can easily exceed supply, with anoxia as the result. In the case of most mud-grade sediments anoxia usually occurs when the volume of dispersed organic carbon exceeds 5% . Where organic carbon occurs as localized con­ centrations (such as macro-organisms), however, the increased mass - surface area ratio inhibits the transfer of oxygen and other electron donors from pore-water solutions . This results in a localized attenuation of bacterial reduction zones, with a reduction 'sink' centred upon the carcase . Thus an anaerobic microenvironment can even be formed in aerated waters if a carcase is big enough . The overall effect of anoxia is to reduce decay rate . This is because anaerobic decomposition of some com­ pounds can only occur after a molecule has been degraded by respiratory processes with higher free­ energy yields (J0rgenson 1982, 1983) . For example, the methanogenic decay of lignified cellulose may require a period of aerobic decay followed by a period of nitrate reduction, then manganese re­ duction, etc. (see Fig . 2, p. 252) . Thus in euxinic environments, where these bacterial reduction zones are severely attenuated (or even absent), the bacterial 'chain' of decomposition is broken and decay rate impaired. Environmental factors such as temperature and pH probably exert most control on decay rate, but they are potentially the most difficult parameters to isolate in the rock record. Increased sediment temperature promotes higher decay rates and an attenuation of the bacterial reduction zones in sedi­ ment. The pH in most sediments is approximately neutral and therefore a suitable environment for microbial respiration. This is not the case in peat swamps, where tannic and fulvic acids liberated by the decomposition of plant material produce an acid environment which halts decay. Soft tissues entombed in such environments become tanned (like leather) and decay resistant. Examples of this type of preservation include the Iron Age 'Bog People' of Northern Europe (Glob 1969), and the Middle Eocene Geiseltalles brown coal from around Halle in East Germany (Allison 1988a) . Details pre­ served include muscle fibres and epithelial cell structure of frogs . Organic carbon in sediment occurs as a variety of complex molecules in association with oxygen, ni­ trogen, hydrogen, and phosphorous . Particular varieties of molecules decay at different rates ac­ cording to molecular configuration and chemical formulae . Those forms which are most amenable to

decay are known as vola tiles, and those which exhibit a degree of decay resistance (and therefore have longer half-lives) are known as refractories . The soft parts of most animals are volatiles and are rapidly decomposed whereas some plant tissues (such as cellulose) are more decay resistant. The decay rate of cellulose, however, is variable and controlled by the presence or absence of other com­ pounds . For example, both lignin (Stout et al . 1981) and certain phenolic compounds (Williams 1963) have been shown to increase the half-life of cellulose if present in decomposing tissue . Effects of decay

Decay is one of the principal sources of information loss in the fossil record . The only way of halting this information loss is by mineralization (Allison 1988a) and a range of preservational characters can be described which reflect diagenetic timing relative to decay (Fig. 1 ) . The highest level of preservation is that of permineralized, volatile, soft tissues such as muscle (for example, mantle muscle of squid from the Jurassic Oxford Clay of Wiltshire, U . K . ; Fig. 2B) . In some circumstances mineral formation occurs after the decomposition of soft tissues but prior to sediment compaction . In this case only the thin, flattened impressions of volatile soft parts are pre­ served (such as in the preservation of soft tissues in siderite nodules from the Carboniferous Mazon Creek fauna of Illinois, U . S . A (Section 3 . 1 1 . 5); Fig. 2B) . If decay further outpaces mineralization, such imprints are destroyed and only refractory tissues such as chitin (from arthropod cuticle) and lignin or cellulose are preserved . These tissues may be pre­ served as permineralizations, altered organic resi­ dues or, with prolonged decay, as impressions . When even these refractories are destroyed, only biogenic hard parts such as bone and shell remain. Decay has considerable impact upon the hydro­ dynamic properties of an organism and this is a further source of preservational bias . A high degree of completeness of soft bodied and lightly skeleton­ ized taxa has been used to infer minimal transport prinr to burial. Such a conclusion is important beG Ise it relates the life habitat of an organism to the � , ·diments in which it was buried . However, a series of tumbling barrel experiments using car­ casses of the polychaete worm Nereis, and the eumalacostracan crustaceans Nephrops and Pal­ aemon have shown that this relationship does not hold (Allison 1986) . The barrel was allowed to rotate at 125 rpm for 5 h, equivalent to turbulent transport

3 . 1 Decay Processes

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Fig. 2 A , Three-dimensional preservation of mantle and appendage musculature in squid from the Jurassic Oxford Clay of Wiltshire, U . K . ; Bristol City Museum, Cb7661 . B, Close-up of muscle fibres in A. C, Flattened polychaete worm from the Upper Carboniferous Mazon Creek biota of Illinois, U.s.A. (A, B from Allison 1988b; reproduced with permission from the Lethaia Foundation. )

for over 1 1 km. Freshy killed organisms subjected to tumbling were hardly damaged (Fig. 3A), while car-

215

casses which had been allowed to decompose for several weeks were disarticulated and fragmented (Fig. 3B) . A sealed glass jar filled with seawater and carcasses of Palaemon was used as a control. The carcasses became buoyed up to the surface with decomposition gases and gradually disarticulated to produce a carpet of skeletal fragments upon the floor of the jar. Thus freshly-killed organisms could tolerate turbulent transport without fragmenting, while at the opposite extreme, carcasses were dis­ articulated when buoyed up by decay gases, even in the absence of currents . It is therefore primarily decay and not transport which determines the degree of fragmentation and disarticulation in soft bodied and lightly skeletonized taxa . Completeness or preservation is therefore no indicator of duration or nature of transport. This interaction between decay and hydrody­ namic processes has produced some difficult taxo­ nomic problems. The most common instance of this form of distortion is provided by fossil plants. A living plant will produce a number of different preservable structures such as pollen, seeds, fruit, and leaves. Upon death, the stem of the plant is commonly fragmented and separated from its root system. Thus, plant fossils are rarely encountered as whole entities . As a result of this bias the remains of most fossil plants are given form names (Section 5 . 1 . 3) . Animal remains too may be subject to this bias. An unusual example is provided by the large Middle Cambrian predator Anomalocaris, from the celebrated Burgess Shale of British Columbia (Section 3 . 1 1 .2) (Whittington and Briggs 1985) . This animal was one of the largest predators of its time, although for many years it was only known from disarticulated elements. The limbs were ori­ ginally identified as arthropod bodies and named Anomalocaris canadensis, while the mouth parts were thought to be a medusoid coelenterate (Peytoia nathorsti) . An incomplete body of the animal was named Lagania cambria and classified as a holo­ thurian . These 'animals' are in fact all part of the same organism. When Anomalocaris died and began to decompose, the mouth parts, body, and append­ ages were separated and deposited according to the hydrodynamic properties of each particular element. The recognition of this decay-induced distortion of fossil taxonomy was only achieved by the discovery of a number of rare complete individuals . The pres­ ervation of complete animals required deposition prior to decay-induced fragmentation. Conversely, the occurrence of disarticulated skeletal elements indicates a period of decay prior to final burial .

216

3 Taphonomy reduction, iron reduction, sulphate reduction, or methanogenesis) used by microbes in the decom­ position process. Sedimentary pyrite, for example, is produced as a by-product of bacterial sulphate reduction (Section 3 . 8 . 3), and manganese carbonates may be produced during manganese reduction (Section 3 . 8 . 2) . Similarly, the fractionation of carbon isotopes during bacterial decay and their incorpor­ ation into the lattice of carbonate minerals is diag­ nostic of specific decay reactions (Coleman 1985) The rarest and most spectacular characterization of decay processes is the preservation of fungi and bacteria in fossil organisms (Allison 1988a) . When bacteria die they undergo autolysis, whereby en­ zymes and other cell contents begin to corrode and eventually destroy the cell wall . Such a process takes hours or days. Thus the mineralization of microbes implies extremely rapid diagenetic growth . Further work on these microbe - carcase associations is required in order to fully understand their significance . References

Fig. 3 Carcasses of Nephrops . A, Freshly-killed individual after tumbling in rotating barrel . Note that although carcase is decapitated, delicate structures such as the appendages have survived . B, Individual tumbled after 26 weeks of decay : a, rostrum; b, c, segments of chelae nearest to coxae; d, pincer; e, mandible; and f, segment of chela attached to pincer.

Characterization of decay

Decay in the fossil record can be characterized on three levels : (1) the identification of information loss and decomposition structures ir, particular fossil organisms; (2) the recognition of particular minerals and geochemical markers associated with particular decay regimes; and (3) the preservation of fossil microbes involved in the decomposition process . The most basic characterization of decay, that of level of preservation in macro-organisms (e . g . per­ mineralized muscle, tissue impressions), merely documents extent of decay prior to mineralization (Figs 1, 2) . A more detailed characterization relates specific geochemical markers to particular decay pathways (i . e . aerobic decay, nitrate reduction, manganese

Allison, P.A. 1986 . Soft-bodied fossils : the role of decay in fragmentation during transport. Geology 14, 979 - 98l . Allison, P.A. 1988a . Konservat-Lagerstatten : cause and classifi­ cation. Paleobiology 14, 331 - 344 . Allison, P.A. 1988b . Phosphatized soft-bodied squids from the Jurassic Oxford Clay. Lethaia 2 1, 403 -410. Coleman, M.L. 1985 . Geochemistry of diagenetic non-silicate minerals: kinetic considerations. Philosophical Transactions of the Royal Society of London A315, 39 - 56 . Glob, P . V . 1969 . The bog people. Faber, London . Jones, G . F . 1969 . The benthic macrofauna of the mainland shelf of Southern California. Allan Hancock Monographs in Marine Biology 4, 1 -219. Jorgenson, B . B . 1982 . Ecology of the bacteria of the sulphur cycle with special reference to anoxic- oxic interface en­ vironments . Philosophical Transactions of the Royal Society of London B298, 543 - 56l . Jorgenson, B . B . 1983 . Processes at the sediment -water inter­ face. In: B. Bolin & R.B. Cook (eds) The major biochemical eye/es and their interactions, pp. 477-561 . John Wiley & Sons, Chichester. Stout, J . D . , Goh, K.M. & Rafter, T.A. 1981 . Chemistry and turnover of naturally occurring resistant organic com­ pounds in soil. Soil Biochemistry 5, 1 - 73 . Whittington, H.B. & Briggs, D . E . G . 1985 . The largest Cambrian animal Anomalocaris, Burgess Shale, British Columbia. Philosophical Transactions of the Royal Society of London B309, 569 - 609 . Williams, A.M. 1963. Enzyme inhibition by phenolic com­ pounds. In: J . B . Pridham (ed . ) The enzyme chemistry of phenolic compounds, pp. 57-85. Pergamon Press, Oxford .

3 . 2 The Record of Organic Components and the Nature of Source Rocks P . FARRIMOND & G . EGLINTON

of the algal material is changed during passage through the gut of the grazing organism; various organic components are preferentially assimilated and modified during digestion, and other lipids may be contributed from tissues of the grazer. An example of this 'editing' process is the observed increase in certain sterols, such as cholesterol (Fig. 1), in faecal pellets of zooplankton fed on phytoplankton (Harvey et al . 1987) . Microbial ac­ tivity, proceeding both in the gut of the feeder and, later, within the faecal pellets, also plays a role in modifying the molecular composition of the organic matter in its descent to the sea floor. Upon arrival at the sediment, organic matter is further modified by a variety of processes acting during early burial. It is during this early diagenesis that biological compounds and debris are incorpor­ ated into insoluble sedimentary organic matter. In addition to the free lipids, the organic matter entering the sedimentary regime comprises bio­ polymers such as carbohydrates, proteins, cutins, and lignins, all of which are available for consump­ tion and modification by benthic macro- and micro­ organisms . There is evidence that a variable fraction of carbohydrates and proteins is initially converted to individual sugars and amino acids by enzymatic microbial attack prior to the use of the resulting monomers by microbes as a source of energy and to form new cell material . The remainder, not utilized in this way, can undergo polycondensation to form geopolymers; these complex, high molecular weight materials may incorporate fulvic and humic acids . This heteropolymeric debris has been termed 'protokerogen' - the precursor of kerogen. With further sediment burial, increasing condensation and insolubilization accompanies the slow dia­ genetic conversion to kerogen, which constitutes the bulk of the organic matter in ancient sediments . Biolipids may be incorporated into kerogen in a similar way, or may be preserved in the sediment with only minor modification . Diagenetic reactions at various stages of burial appear to convert some lipids to hydrocarbons (Fig. 1) through the loss of functional groups via dehydration, hydrogenation,

Preservation and diagenesis

Organic molecules are abundant constituents of many sediments and sedimentary rocks . These components have been referred to as 'chemical fossils' in recognition of their biological origin, but the terms 'biological marker' or simply 'biomarker' are more commonly used . Macro- and micro fossils are readily apparent in rocks, but the identification of chemical fossils requires sophisticated techniques of sample work-up and analysis; nevertheless, they too preserve a remarkably detailed record of past biological activity. 'Biological markers' are defined as organic compounds present in sediments (or petroleums) which possess chemical structures un­ ambiguously related to present day biologically­ occurring organic molecules (Fig. 1 ) . Obviously, the possible sources of biomarkers in geological samples are almost limitless, comprising all organisms in the palaeoenvironment of deposition - aquatic, land, and air . Consequently, the molecular record is in­ variably complex. Furthermore, numerous chemical reactions, both biologically and non-biologically mediated, proceed within the water column and then during sedimentation and burial of the organic debris; these serve to modify and diversify the record of organic components still further. Only a relatively small proportion of the organic matter produced within, or supplied to, ocean sur­ face waters ever reaches the underlying sediments; the vast proportion of this material is recycled (much of it 'remineralized' to carbon dioxide) within the water column, particularly in the euphotic zone . Many processes act to modify the organic flux, including photo-oxidation, microbial activity, and predation by grazing organisms. Of the very small fraction of the original marine organic material which arrives at the sediment, a large proportion is generally transported in the form of faecal pellets released by zooplankton or organisms higher in the food chain. Such faecal pellet transfer is relatively rapid, allowing marine organic matter produced in the euphotic zone largely to escape photo-oxidative degradation . However, the molecular composition

217

3 Taphonomy

218

BIOLlPID

GEOLl PID

HO C h o lesterol

S a ( H ) -C h o l esta n e

Po r p h yr i n C h l o ro p h y l l a

OH

OH

OH Bacte r i o h o pa n etetro I

C35 H o p a n e

and decarboxylation. Such hydrocarbons cannot be readily incorporated into geopolymers by poly­ condensation reactions . However, a proportion may become trapped in the kerogen structure . The remaining free hydrocarbons and other related compounds comprise only a small proportion of the organic matter in a sediment (typically less than 5%), although they have a high information content. These 'chemical fossils' have been introduced into the sediment from their source organisms with only relatively minor changes to their molecular structure . It is only through knowledge of the reactions proceeding during sedimentation of organic matter through the water column, and during its sub­ sequent burial in the sedimentary record, that

Fig. 1 Three biologically widespread molecules and their geologically occurring products after diagenesis . Note that, in each case, structural specificity is maintained - the geolipids are thus 'chemical fossils', having an unambiguous link with their precursor biolipids .

geologically-occurring lipids may be used as a source of information . Certain lipid classes, notably the steroids (Mackenzie et al. 1982), are becoming well understood in this respect, although other classes await study. A knowledge of precursor ­ product relationships allows the use of sedimentary organic components as indicators of biological sources of organic matter, depositional environment or conditions, climatic variations, and organic matter maturity. Biological marker compounds and their uses

Biological marker compounds have a wide variety of structures, all specifically indicative of a biological origin. The degree of specificity in the structure

3 . 2 Organic Components and Source Rocks may enable inferences to be made as to the precursor molecules, and hence the ultimate origin in a par­ ticular family, class, or even genus of organism (see also Section 2 . 1 ) . Of course, detailed chemotaxo­ nomic information for modern organisms is the essential basis for successful correlation with such biological sources . Furthermore, when applying biomarkers as source indicators in ancient sedi­ ments it is necessary to make the major assumption that ancestor organisms possessed similar molecular compositions to their modem descendants . How­ ever, there are often good biosynthetic grounds for such assumptions . Obviously, it is desirable for links to be established between specific fossils (macro and micro) and the molecular record. For example, what does the brown or black material comprising a leaf fossil really consist of? Is there a molecular record of the original lignin, cutin, or wax? Similar questions apply to other macrofossils (e .g. fish re­ mains) and microfossils . Unfortunately such work is only in the early stages . Nevertheless, despite these constraints, a considerable number of indica­ tive compounds, and, indeed, classes of compound, are generally accepted as reflecting certain biological inputs, as discussed below. These and other bio­ logical markers are reviewed by Brassell et al. (1978) and Philp (1985) . Straight-chain alkanes (n-alkanes) and their func­ tionalized equivalents (n-alcohols (alkanols), n-fatty acids (alkanoic acids), and n-alkanones) are common constituents of the majority of organisms (e . g . leaf waxes of higher plants, membrane lipids of algae, etc . ) . In addition, the distributions of carbon chain lengths of these compounds are informative as to the origin of organic matter in a sediment. In gen­ eral, short- (C 1 S - C 1 9) and medium-chain (C20 - C24) compounds reflect algal and/or bacterial sources, whilst long-chain compounds (C27-C33) typify a higher plant contribution. A class of organic compounds known as hopa­ noids are ubiquitous constituents of sediments . Several biological precursors of the geological hop­ anoids have been identified - almost all are bac­ terial in origin (Fig. 1 ) . More specific biological marker compounds have also been proposed . For example, certain long-chain acyclic isoprenoids are common constituents of archaebacteria; further­ more, some compounds appear to be restricted to methanogens (Brassell et al. 1981 ) . Other widely accepted biological marker compounds include 18<x(H)-0Ieanane (higher plants), 4-methylsteroids (especially dinosterol; dinoflagellates), long-chain alkenones (prymnesiophyte algae), and botryo-

219

coccane or botryococcenes (only observed in the fresh- or brackish-water alga Botryococcus braunii) . An appraisal of the biological sources of the sedi­ mentary organic matter, and the relative importance of specific contributions, aids the reconstruction of the environment of deposition of the sediment. For example, freshwater and marine sediments may usually be distinguished by their molecular signa­ tures, owing to the contribution of organic matter from different organisms in the two environments . Furthermore, in the marine realm, the abundance of terrestrial organic matter is related to proximity to land and the importance of fluvial and/or aeolian transport of land-plant debris . In petroleums, the molecular composition is the best (if not the only) source of information regarding the environmental setting of its source rock. In addition to providing clues to the broad depo­ sitional setting of a sediment, the molecular record is instructive with regard to the environmental conditions prevailing at the time of deposition . Of prime concern here is the oxicity of the water column . Didyk et al. (1978), in an extension of the work by Powell & McKirdy (1973), proposed the ratio of two related organic compounds, pristane and phytane, as an indicator of oxygen levels at the site of deposition . Whilst the basic rationale behind this indicator is sound - namely two different reaction pathways from the same precursor (the phytol side chain of chlorophyll; Fig. 1), the one followed being dependent upon the oxygen level of the environment - the effects of differences in organic matter sources and maturity complicate its use . However, when used in conjunction with other evidence, such as porphyrin content, this ratio can be a useful indicator of the degree of oxygenation. Sediments deposited in hypersaline environ­ ments are frequently characterized by distinctive distributions of biomarkers (ten Haven et al . 1988) . These unusual molecular signatures presumably reflect a contribution of organic matter from salinity­ tolerant organisms, coupled with the presence of highly reducing conditions of deposition . During sediment burial and organic matter matu­ ration, biological marker distributions are modified through chemical reactions . Whilst early diagenesis is characterized mainly by reactions involving the loss of functional groups, during late diagenesis and catagenesis the biomarker reactions are domi­ nated by isomerization and degradation processes (Mackenzie et al . 1980) . Each reaction proceeds over a specific range of maturity, dependent upon time, temperature, and to a lesser extent, pressure (Tissot

220

3 Taphonomy

& Welte 1984) . Consequently, determination of the extent of such reactions in a sediment (typically by molecular product- precursor ratios) allows the assessment of maturation stage - critical in oil generation studies . A further application of the molecular components of sedimentary organic matter lies in the recon­ struction of palaeoclimatic fluctuations . Recent progress in this area includes the recognition of a molecular 'palaeothermometer' in a group of organic compounds called alkenones (Brass ell et al. 1986) . A simple molecular parameter is now available which can be used to illustrate past fluctuations in sea­ surface temperatures, as prymnesiophyte algae modify their molecular composition in response to long-term temperature changes . This approach is currently being employed to record glacial or interglacial cycles in deep-sea sediment cores, and compares well with classical oxygen isotope measurements on foraminifera . Biological marker compounds may also record marine productivity changes, and variations in aeolian transport of terrestrial organic debris.

The nature of source rocks

Exactly what constitutes a hydrocarbon source rock has long been a matter of debate, although advances in petroleum geology and geochemistry have re­ sulted in the general acceptance of a broad defi­ nition. Brooks et al . (1987) define a source rock as 'a volume of rock that has generated or is generating and expelling hydrocarbons in sufficient quantities to form commercial oil and gas accumulations' . A potential source rock is a volume of rock which has the capacity to generate commercial hydrocarbon accumulations, but is of insufficient maturity. Most source rocks are fine-grained, typically dark­ coloured shales or marls . However, the organic matter within a sediment must meet minimum re­ quirements for organic richness and quality or type in order for the rock to be considered a source bed . Most potential source rocks contain between 0 . 8 and 2 % organic carbon; an approximate limit of 0 .4% is commonly accepted as the lowest organic carbon content for hydrocarbon generation and expulsion to occur. Of course, there is no general upper limit of organic richness, and many of the best source beds contain upwards of 5 - 10% organic carbon. The kerogen in a source rock may contain par­ ticulate organic matter from a variety of sources in fact, the nature of the hydrocarbons generated is

strongly dependent upon the kerogen composition . Most kerogens are mixtures of two types of organic matter: terrigenous higher plant debris and aquatic (marine or lacustrine) lower plant material. Micro­ scopic analysis of source rocks reveals that most of the sedimentary organic matter is amorphous, with only a minor part comprising recognizable biologi­ cal debris. Sediments containing large quantities of yellow-brown amorphous organic matter of algal and/or bacterial origin (i . e . types I or 11; Tissot & Welte 1984) will produce petroleum given sufficient maturation. In contrast, sediments containing type III kerogens, comprising abundant particulate land plant debris, will liberate mainly gas . There are two main prerequisites for the ac­ cumulation of significant quantities of organic matter in sediments : production of organic matter, and its subsequent preservation . Both are controlled by many variable factors (Fig. 2) .

Production of organic matter. Source rocks may be deposited in marine or lacustrine environments . Owing to their greater importance, only marine source rocks will be discussed here, although many of the factors controlling organic matter accumu­ lation apply in both environments . Marine primary productivity typically supplies the bulk of organic matter to marine source rocks, although processes within the water column utilize much of the organic debris before it can reach the sediment. Surface productivity is largely controlled by water temperature, light intensity, and the avail­ ability of nutrients . The latter may be influenced by sea-level (with the flooding of coastal areas during periods of high sea-level introducing terrigenous nutrients), water column overturn (resulting from storm activity or improved deep circulation), and up welling of nutrient-rich water. Upwelling is, in turn, controlled by the action of prevailing winds and the Earth's Coriolis forces, and by the distri­ bution of land masses . Present-day upwelling areas overlie many of the most organic-rich sediments in the oceans. Terrigenous higher plant debris, which may also be a significant constituent of hydrocarbon source rocks, may be introduced into the marine environment by flooding of coastal areas during transgression, or by aeolian or fluvial transport.

Preservation of organic matter. The accumulation of organic debris in sediments depends to a large extent upon the inhibition of chemical oxidation and biochemical degradation processes during transport, deposition, and early burial . These pro-

221

3 . 2 Organic Components and Source Rocks

Terrest rial influx of o rga n i c matter

Water tem pe r ­ atu re

co l u m n stratificati o n

Balance o f evaporation vs. prec i p i tation

Fig. 2 Flow diagram showing various interrelated factors which influence the production of organic matter in the biosphere, and its subsequent preservation in the geosphere . These factors may all exert some control upon the accumulation of organic matter in marine sediments .

cesses, in turn, depend upon sediment particle size, sedimentation rate, mode of transport of organic matter to the sediment, and water column oxicity. Thus, organic-rich sediments are typically fine­ grained, and are favoured by relatively high sedi­ mentation rates, resulting in rapid burial. Rapid transit of organic debris through the water column, either through faecal pellet transport or sediment re deposition (turbidity currents, etc . ), also favours organic matter preservation. However, the oxicity of the water column, particularly at the sediment surface where residence time of organic matter is generally high, has long been recognized as the major control on the preservation of organic carbon in sediments . Under oxygen-depleted conditions, aerobic bacterial activity is absent, and degradation of organic matter is limited to the action of the less efficient anaerobic bacteria (see also Section 3 . 1 ) . Furthermore, the grazing o f macro-organisms on the sediment surface ceases in low-oxygen con­ ditions; consequently, there is no bioturbation to promote the access of oxygen and aerobic bacterial degradation within the upper sediments . The resulting sediments are usually finely laminated,

and typically contain relatively large amounts of organic matter. The oxygen content at any point in the water column is controlled by oxygen demand (which is controlled by organic matter degradation), oxygen supply, and oxygen solubility (which is greatly reduced in warmer or more saline water) . Oxygen supply in the marine environment is largely a func­ tion of deep-water circulation, although oxygen is supplied to surface waters by exchange with the atmosphere and photosynthetic production. Demaison and Moore (1980) discussed several models for the deposition of oil source beds - all involving highly oxygen-depleted conditions . One such model is that of a restricted and/or stratified basin. Oxygen-deficient conditions may develop in sedimentary basins where physical barriers tend to inhibit water circulation, particu­ larly in basins with a positive water balance (i. e . river inflow exceeding evaporation) . The present­ day Black Sea is a much-cited example of an anoxic silled basin with organic-rich sediments . Depo­ sition of potential source beds is also favoured in permanently stratified lakes (e . g . Lake Tanganyika) .

222

3 Taphonomy

Density stratification in basins may be induced by the influx of dense, oxygen-poor, saline water (formed in shelf areas where evaporation is high), or by the influx of low density freshwater (in areas of high precipitation) . Such stratification in the water column inhibits circulation, and hence oxygen replenishment is poor. The second type of oxygen-deficient environment where organic-rich sediments are characteristic is that of an expanded mid-water oxygen-minimum layer. The best developed of these form in response to coastal upwelling of nutrient-rich waters in areas where oxygen supply cannot match demand as or­ ganic matter degrades in the water column (e . g . Peru Upwelling) . Alternatively, oxygen-minimum layers may develop in areas where productivity is normal, but oxygen supply is poor due to isolation from a source of well oxygenated water. In either case, organic-rich sediments may be deposited where the oxygen-minimum layer impinges upon a continental slope or shelf. Open ocean oxygen minima, covering wide areas of the oceans, may have been important during specific times in the past - the so-called 'oceanic anoxic events' . These relatively short periods of geological time were characterized by widespread accumula­ tion of organic-rich sediments . The best known examples occur in the Cretaceous (Aptian ­ Albian, Cenomanian -Turonian, and Coniacian ­ Santonian), although another well defined oceanic anoxic event occurs in the Toarcian Gurassic) . Organic-rich sediments from these intervals com­ prise a large proportion of the world's potential and actual source rocks . References Brassell, S . c . , Eglinton, G . , Maxwell, J.R. & Philp, R.P. 1978. Natural background of alkanes in the aquatic environ­ ment . In: O. Hutzinger, L H . van Lelyveld & B . C .J . Zoeteman (eds) Aquatic pollutants : transformation and bio-

logical effects, pp . 69 - 86. Pergamon Press, Oxford . Brassell, S . c . , Eglinton, G . , Maxwell, J.R. Thomson, L D . & Wardroper, A.M.K.' 1981 . Specific acyclic isoprenoids as biological markers of methanogenic bacteria in marine sediments. Nature 290, 693 - 696. Brassell, S . c . , Eglinton, G . , Marlowe, L T . , Pflaumann, U. & Sarnthein, M. 1986. Molecular stratigraphy: a new tool for climatic assessment . Nature 320, 129 - 133. Brooks, J., Cornford, C. & Archer, R. 1987. The role of hydro­ carbon source rocks in petroleum exploration . In: J. Brooks & A.J. Fleet (eds) Marine petroleum source rocks, pp. 17-46. Special Publication of the Geological Society of London No . 26. Blackwell Scientific Publications, Oxford. Demaison, G.J. & Moore, G.T. 1980 . Anoxic environments and oil source bed genesis . Organic Geochemistry 2, 9 - 31 . Didyk, B . M . , Simoneit, B . R T. , Brassell, S . c . & Eglinton, G . 1978. Organic geochemical indicators o f palaeoenviron­ mental conditions of sedimentation. Nature 272, 216-222. Harvey, H.R., Eglinton, G., O'Hara, S . C . M . & Corner, E . D . 5 . 1987. Biotransformation and assimilation of dietary lipids by Calanus feeding on a dinoflagellate . Geochimica et Cosmochimica Acta 51, 3031 - 3040 . Haven, H . L . ten, de Leeuw, J.W. & Sinninghe Damste, J . S . 1988. Application o f biological markers i n the recognition of palaeo-hypersaline environments . In: A.J. Fleet, K . Kelts & M.R. Talbot (eds) Lacustrine petroleum source rocks . Special Publication of the Geological Society of London, No . 40, pp . 123 - 140 . Blackwell Scientific Publications, Oxford. Mackenzie, A.5., Patience, R.L., Maxwell, J.R., Vandenbroucke, M. & Durand, B. 1980. Molecular para­ meters of maturation in the Toarcian shales, Paris Basin, France - L Changes in the configurations of acyclic isoprenoid alkanes, steranes and triterpanes. Geochimica et Cosmochimica Acta 44, 1709 - 1 721 . Mackenzie, A . 5 . , Brassell, S . c . , Eglinton, G. & Maxwell, J.R. 1982. Chemical fossils - the geological fate of steroids. Science 217, 491 - 504. Philp, R.P. 1985 . Biological markers in fossil fuel production. Mass Spectrometry Reviews 4, 1 - 54. Powell, T.G. & McKirdy, D.M. 1973. Relationship between ratio of pristane to phytane, crude oil composition, and geological environment in Australia. Nature, Physical Sciences 243, 37-39. Tissot, B . P . & Welte, D.H. 1984. Petroleum formation and occurrence, 2nd Edn . Springer-Verlag, Berlin.

3 . 3 Destructive Taphonomic Processes and Skeletal Durability C . E . B RE T T

Destructive processes

evidenced by decay experiments using controls in cages that exclude larger organisms . Scavenging and burrowing processes are precluded in anaero­ bic environments, thus favouring articulated pres­ ervation. Physical agents, such as current and wave turbu­ lence, also produce disarticulation in skeletons which have undergone some decay. It is frequently assumed that the transport of carcasses over any distance will result in their disarticulation. How­ ever, if organisms are transported just prior to death, or immediately thereafter, this may not be the case (Allison 1986; Section 3 . 1 ) . Conversely, once connective tissues have decayed, even very minor currents (less than 5 cmls) may be effective in producing complete disarticulation . Interlocking structures of skeletons inhibit disar­ ticulation. For example, the interlocking hinge-teeth of certain brachiopods (such as terebratulids) may prevent disarticulation of the valves for extended periods of time . The tightly crenulated sutures of some pelmatozoans and echinoids appear to be similarly resistant. Thus, most multielement skeletons can only be preserved as articulated remains if they are buried extraordinarily rapidly (hours to a few days) . Anoxic environments promote articulated preservation, as does an absence of turbulence . However, these fac­ tors are not sufficient in themselves to explain this mode of preservation . Tightly sutured skeletons (e . g . the tests of echinoids, and crinoid stems), on the other hand, may withstand much longer periods of exposure in marine environments .

Durability refers to the relative resistance of skel­ etons to breakdown and destruction by physical, chemical, and biotic agents . The processes of skel­ etal destruction can be subdivided into five cat­ egories which follow one another, more or less sequentially, as remains of organisms are exposed in different environments (Seilacher 1973; Muller 1979; Brett & Baird 1986) : (1) disarticulation; (2) frag­ mentation; (3) abrasion; (4) bioerosion; and (5) corrosion and dissolution. Depending on the physi­ cal characteristics of the sedimentary environment, one or more of these processes may be more active . 1

Disarticulation is the disintegration of multiple­ element skeletons along pre-existing joints or articulations . There is a paucity of hard data on disarticulation rates, although this has been partly alleviated by several observational and experimental studies (Schafer 1972; Allison 1986, 1988; Meyer & Meyer 1986; Plotnick 1986) . Disarticulation may occur even prior to death in the case of moulting, which yields recognizable exuviae in many arthro­ pods. In most cases, disarticulation proceeds very rapidly after the death of an organism, and may in­ volve biochemical breakdown of tissues by enzymes present in the body of the organism itself. Bacterial decay (see also Section 3. 1) of ligaments and con­ nective tissues proceeds at a variable rate depending upon the nature of the tissues, as well as the local environment of decay. Aerobic decay of tissues proceeds rapidly in most cases; e . g . , the ligaments binding echinoderm ossicles are broken down within a matter of hours to a few days after death . Hinge ligaments composed of conchiolin in bivalves are evidently more resistant, and can remain intact for periods of months, despite fragmentation of the shells. Anoxia obviously inhibits bacterial decay. None the less, recent experiments indicate that anaerobic bacteria destroy ligaments and connective tissues within a matter of a few weeks to months . Biotic agents, including scavengers and infaunal burrowers, may greatly accelerate disarticulation as

2

Fragmentation of skeletons results both from physical impact of objects and from biotic agents such as predators and scavengers . Some fragmen­ tation may occur prior to death, such as that pro­ duced by attempted predation (see also Section 4. 13) . Distinct fragments or patterns of breakage may be recognizable in certain instances, e . g . the curved fractures produced by peeling of gastropod apertures by crabs. However, more commonly, pre223

224

3 Taphonomy

dation damage is indistinguishable from physical breakage . Shells tend to cleave along pre-existing lines of weakness such as growth lines, or ornamentation such as ribbing, and yield consistent types of frag­ ments (Fig. 1 ) . Resistance to fragmentation relates to several aspects of skeletal morphology and com­ position, including thickness and curvature of shells, microarchitecture, and percentage of organic matrix. In general, nacreous (pearly) skeletal fabric in mollusc shells are most resistant to breakage by impact, whereas foliated shells are more fragile . Bacterial decomposition of organic matrix greatly weakens shells, and makes them much more sus­ ceptible to fragmentation by other agencies; hence, for example, the high organic content of the shells of certain nuculid bivalves has probably resulted in their under-representation in the foss�l record . Sur­ ficial exposure time is also critical; microborings of endolithic algae and fungi greatly weaken shell structure and facilitate breakage . Delicate skeletons of corals, bryozoans, graptolites, and other fossils are particularly prone to fragmentation, even in slightly agitated waters . Hence, they form key taphonomic indicators of changes in current energy among facies . A high degree of fragmentation sug­ gests persistent breakage and reworking, perhaps within normal wave base . Extraordinary events, such as storms, may also generate currents or waves that impinge on otherwise quiet environments and cause intermittent fragmentation.

3 Abrasion, or physical grinding and polishing, results in the rounding of skeletal elements and loss of surficial details (Fig. lE). The extent of abrasion in any given type of skeleton is related to environ­ mental energy, exposure time, and particle size of the abrasive agent. In general, the rate of abrasion increases with increasing grain size: clay-sized grains do not significantly abrade skeletons; sand­ and gravel-sized material is probably the most effective agent. Semiquantitative measurements of abrasion rates have been obtained by tumbling shells artificially (Fig. 2; Chave 1964) . Two factors strongly influence the relative resistance of skel­ etons : size relative to the grain size of the sediment, and microarchitecture . Not surprisingly, small bi­ valve shells are fragmented and abraded much more readily than large ones. Furthermore, dense skeletal microstructures, such as crossed-lamellar structure in molluscs, are relatively hard and resistant to abrasion. Gastropods with dense shells may survive over one thousand hours of continuous tumbling.

B Fig. 1 A, Abrasion and breakage may produce fragments diagnostic of different depositional environments. Stably anchored shells are abraded from the top down (anchor faceting) . Pounding of shells by surf produces fractures that follow medial and concentric lines of weakness in the shell. Rolling and gliding of the shell will abrade the outer edge (glide faceting) . B, Roll fragments are produced by shells tumbling in an abrasive medium which preferentially destroys thinner parts of the shell, leaving thickened umbonal parts intact: spiriferid brachiopods from the Lower Devonian Oriskany Sandstone of Maryland. (After Seilacher

1973 . )

Moderately porous and/or organic-rich shells dis­ play intermediate durabilities, while very porous skeletons, such as those of bryozoans and algae, abrade very rapidly and will be selectively removed from the fossil record of high energy environments . However, porous particles such a s echinoderm os­ sicles may be cushioned against abrasion by their low density . Thus, it is commonly assumed that echinoderm ossicles can be strongly abraded only if they have undergone some early diagenetic permineralization .

4 Bioerosion, commonly associated with recogniz­ able trace fossils such as the borings of clionid sponges and various endolithic algae, proceeds at

225

3 . 3 Skeletal Durability

1 00�-------r--r---1

Fig. 2 Durability of invertebrate skeletal material in a tumbling barrel filled with chert pebbles. Numbers following each skeleton name give the initial size range in centimetres . (After Chave 1964; reproduced with the permission of John Wiley & Sons, Inc . )

o

Cor a l l i n e �AlgQe

very high rates in most shallow-marine environ­ ments . Rates from 16% to over 20% weight loss per year, as a result of algal and sponge boring, have been observed for modern marine mollusc shells. It is not clear whether such rates pertained in the Palaeozoic when clionid sponges were much less abundant. As with abrasion, shell thickness, organic content, and perhaps density may influence the relative resistance of skeletal material to destruction by bioerosion. 5

1 00

1

Corrosion and dissolution of skeletons result from chemical instability of skeletal minerals in seawater or in sediment pore-waters . Dissolution may begin at the sediment- water interface and continue to considerable depths within the sediment. Biotur­ bation of sediments commonly promotes dissol­ ution by the inmixing of fresh seawater and by oxidation of sulphides to produce weak acids within sediment pore-waters . A general ordering of the stability of minerals is as follows : phosphate > silica > echinoderm calcite > other skeletal calcite > aragonite . In addition, skeletal materials containing a high proportion of organic matter, such as nacreous shell, are relatively more resistant to dissolution than those with pure carbonate mineralogies, a trend which runs counter to destruction by abrasion or fragmentation. This differential stability results in biases in the records of different groups: e . g . , calcitic brachiopod shells may be extremely well preserved where aragonitic molluscs occur as highly compacted internal ­ external moulds. In practice, the effects of mechanical abrasion, most bioerosion, and corrosion are difficult to dis­ tinguish in fossils . Hence, Brett and Baird (1986) suggested the use of the term corrasion to indicate the general state of wear in shells resulting from any

1 000

T I M E I N H O U RS ( l o g sca l e )

combination of these processes . Corrasion provides a general index of exposure time to various agencies of wear on the sea floor.

Skeletal durability

Destructive processes of disarticulation, fragmen­ tation, and corrasion are readily evident in the fossil record. These processes affected different skeletal types in different ways . Most marine skeletonized organisms can be assigned to one of five skeletal architectural categories : massive, arborescent, uni­ valved, bivalved, or multielement. Table 1 provides a summary of biostratinomic processes, such as fragmentation and disarticulation, with respect to their influence upon each of the five skeletal types . I n general, massive skeletons are the least subject to breakage and are most resistant to mechanical destruction. However, because they remain on the sea floor for prolonged spans of time, such massive skeletons often display the effects of corrasion to a greater extent than other skeletons. Arborescent skeletons are probably the most sensitive indicators of fragmentation; an absence of breakage in such skeletons is an excellent indicator of minimal dis­ turbance of the sedimentary environment. Most bivalved skeletons become disarticulated relatively rapidly after death, although those with tough con­ chiolin ligaments may remain articulated for exten­ sive periods . Finally, multielement skeletons provide the best indicators of rapid burial, as they disarticu­ late extremely rapidly in the absence of sediment cover. Taken together, various skeletal types and their varied sensitivities to destructive agents may provide excellent indicators of sedimentary pro­ cesses, and can be used to define taphonomic facies (Section 3 . 9) .

3 Taphonomy

226

Potential utility of various invertebrate skeletal types as qualitative indicators of physical environmental parameters . In each case the types of evidence useful for inferring a given condition (e . g . high energy) are listed as symbols, defined at the bottom of the table . (From Brett & Baird 1986.)

Table 1

Current/wave transport of skeletons

Skeletal type

Azimuthal (compass-bearing) orientation

Burial rate

Environmental energy

Convex up/down

Low

Single unit Massive

High

Slow, reworked

++

++

(do)

(cor)

Very rapid

++

Encrusting

(cor) Ramose, robust Ramose, fragile Univalved shell

Multiple unit Bivalved shell, thick Bivalved shell, thin Multielement, tightly sutured Multielement, loosely articulated

+

+

+

++

(la)

(fr)

(fr)

(cor)

++

+

+

(la)

(fr)

(fr)

++

+

+

+

(la, d)

(do)

(cor)

(fr)

+

+

+

+

+

+

(la)

(do)

(fr)

(fr)

(fr, cor)

(da)

+

++

++

+

(la)

(do)

(da, fr)

(fr)

+

+

+

+

+

(la)

(da)

(da, fr)

(da, cor)

(da)

+

++

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(la)

(da)

(da)

Utility as indicator of given condition: - not generally usable; + usable indicator; Type of indicator: cor = degree of corrosion; do = disorientation (overturning); fr articulation; la = long axis lineation; d = direction of apex .

References Allison, P.A. 1986 . Soft bodied animals in the fossil record: the role of decay in fragmentation during transport. Geology 14, 979 - 981 . Allison, P.A. 1988 . The role of anoxia in the decay and mineralization of proteinaceous macro-fossils . Paleo­ biology 14, 139 - 1 54 . Brett, c . E . & Baird, G . c . 1986. Comparative taphonomy : a key to paleoenvironmental interpretation based on fossil preservation. Palaios 1, 207- 227. Chave, K.E. 1964. Skeletal durability and preservation. In: J . Imbrie & N.D. Newell (eds) Approaches to paleoecology, pp. 377- 387. Wiley, New York. Meyer, D . L . & Meyer, K.B. 1986. Biostratinomy of Recent

++ =

very important indicator. fragmentation (or lack of); da

=

. . . disarticulation!

crinoids (Echinodermata) at Lizard Island, Great Barrier Reef, Australia. Palaios 1, 294- 302. Miiller, A.H. 1979 . Fossilization (taphonomy) . In: R.A. Robison & C . Teichert (eds) Treatise on invertebrate paleontology. A, fossilization (taphonomy), biogeography, and biostratigraphy, pp. A2 -A78 . Geological Society of America, Boulder, and Kansas University Press, Lawrence . Plotnick, R.E. 1986. Taphonomy of a modern shrimp : impli­ cations for the arthropod fossil record. Palaios 1, 286-293. Schafer, W. 1972. Ecology and paleoecology of marine environ­ ments . University of Chicago Press, Chicago . Seilacher, A. 1973. Biostratinomy: the sedimentology of bio­ logically standardized particles . In : R. Ginsburg (ed . ) Evolving concepts in sedimentology, pp. 159 - 1 77. Johns Hopkins University Studies in Geology No. 21 .

3 .4 Transport - Hydrodynamics

and unpredictable, chiefly because of the huge di­ versity of forms involved . The s h ell properties of greatest influence are : (1) the kind and degree of symmetry; (2) the degree of elongation; (3) the degree of shell curvature (brachiopods, bivalve mol­ luscs, ostracodes) or the apical angle (gastropods); (4) the character and distribution of ornament and the presence of teeth or processes along the hinge (brachiopods, bivalve molluscs); (5) the mean mass per unit shell area; and (6) the distribution of mass. Aside from fluid properties, the other factors con­ trolling behaviour are : (7) the agent transporting the shell (river, tidal stream, waves, turbidity cur­ rent); (8) the force exerted by the agent; (9) the nature of the bed on which the shell alights or over which it moves; and (10) the character and distribution of any other particles, either already deposited or moving with the shell . The ultimate response of the shell is to assume a characteristic attitude and orientation on the sedimentary surface; these properties, when summed over a sample of shells, constitute a biofabric (Kidwell et al. 1986; Section 3 . 5), which may be diagnostic of current direction and/or agency. Attitude, whether concave­ up or convex-up, is especially important in the analysis of transported brachiopod, bivalve mollusc, and ostracode valves . Introducing the pointing di­ rection afforded by an apex or umbone, shell orien­ tation may be measured with respect to either the axis of symmetry of the shell (gastropods, ortho­ cones, belemnite guards, crinoid columnals) or some convenient feature such as the line of elongation, the hinge, or a straight edge (brachiopods, bivalve molluscs, ostracodes) .

3 . 4 . 1 Shells J . R . L . ALLEN

Introduction

A consideration of the following as sedimentary particles exemplifies the range of behaviour of shelly hard parts: the shells of brachiopods, bi­ valve, gastropod and cephalopod molluscs (includ­ ing those with internal hard parts), ostracodes, and articulated crinoid columnals . All but the crinoids typically have hard, calcareous coverings marked by a low mass per unit surface area . The brachiopods are protected by two normally unequal but bilater­ ally symmetrical opposed valves, which may separ­ ate after death on the decay of muscle tissue . Equal but asymmetrical (about the umbone) valves typify the bivalve molluscs; separation depends on the decay of the ligament. In the brachiopods, and particularly in the bivalve molluscs, there may be teeth and other processes projecting from the hinge . Typically, gastropods have spiral shells with a wide range of apical angle and external ornament, which approximate to axial symmetry. External shells in the cephalopods are chambered and vary from straight (axially symmetrical) to more or less tightly coiled (bilaterally symmetrical) . The internal shell of the coleoid cephalopods varies from straight and axially symmetrical (e . g . belemnite guards) to flattened with bilateral symmetry (cuttlefish) . Ostracode valves are equal, but not symmetrical normal to the hinge . Articulated crinoid columnals are axially symmetrical and virtually cylindrical. Little is understood of the hydrodynamic behaviour of these hard parts, so abundant and ecologically important in modern shallow-water environments and the fossil record . Field studies are few (Nagle 1967; Salazar-Jimenez et al . 1982) and what laboratory experimental work exists (Kelling & Williams 1967; Brenchley & Newa1l 1970; Futterer 1978; AlIen 1984) seldom faithfully reflects natural conditions. There is a particular paucity of data on the behaviour of shells en masse. The hydrodynamic behaviour of shells is complex

Settling

Shells will eventually settle to the bed after having been either carried from shallow- to deep-water by turbidity currents or swept up into the water column by storm waves on a shelf. Laboratory experiments give some insight into the settling of bivalve mollusc valves . A terminal settling velocity i s reached when the upward drag acting on the sinking shell equals the downward-acting immersed weight. Valves of all studied species eventually fall concave-up (Fig. lA) .

227

228

3 Taphonomy

The centre of mass of the shell then lies below the centre of fluid force, there being no turning couple. Released convex-up, a turning couple at once ap­ pears because, in this attitude, the centre of action of the prevailing fluid forces underlies the centre of particle mass (Fig . lE). Valves with a length similar to the height sink steadily on a helical path, the shell spinning once about a vertical axis for each turn of the trajectory (Fig . IC) . The sense of the trajectory, either clockwise or anti-clockwise, varies with the species and whether the valve is on the left or the right. Valves with a length more than about 1 . 6 times the height settle unsteadily, the shell dis­ playing a regular oscillation (pitching), amongst other motions, while settling either spirally or irregularly (Fig. ID) . The drag coefficient of sinking mollusc valves is invariably substantially larger than for dynamically equivalent smooth spheres (i. e . those with the same

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Some understanding of the complex process of transport in one-way currents has come from field observations and laboratory experiments, but much remains unknown, particularly concerning shells in bulk. In the case of dispersed bivalve molluscs, entrain­ ment depends on the orientation and particularly the attitude of the shell, and on the roughness of the

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balance of inertial and viscous forces) . Valves that settle unsteadily differ most from spherical particles, affording drag coefficients up to three times greater. Thus the 'quartz equivalents' (the size of a quartz grain or pebble with the same terminal settling velocity) of mollusc valves are much smaller than the valves themselves .

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Fig. 1 Schematic summary of the behaviour and idealized biofabrics of representative shells (bivalve molluscs (Cerastoderma, Mytilus); gastropods (Turritella); belemnite guards) when settling in water, and when transported and deposited from one-way and oscillatory currents .

3 . 4 Transport - Hydrodynamics bed relative to the scale of the valves . For planar beds of particles much smaller than the valves, convex-up shells require a larger fluid force for entrainment than concave-up ones, the force for convex-up entrainment varying from a few to many times greater, depending on shell shape and mass per unit area. Hence the drag coefficient of a convex­ up valve is smaller than for the same valve when concave-up; consequently a given valve is most streamlined when convex-up (Fig. lE). Once entrained, convex-up valves take a variety of orien­ tations depending on shell shape and the promi­ nence and distribution of teeth and other processes along the hinge, which can act like a storm anchor (Fig. IF, G) . Convex-up valves tend, without change of attitude, to glide over relatively immobile planar beds, but on mobile, sandy ones they may speedily become partly buried and thus halted. Concave-up valves entrained on relatively fine-grained planar beds also maintain their attitude while gliding over the bed but become tilted downcurrent. Overturn­ ing into the more resistant and stable convex-up position occurs only where the moving valve en­ counters a substantial obstacle on the bed. An ex­ ception is the stout-shelled Mytilus edulis, valves of which at once turn over when entrained from the concave-up attitude . As natural beds abound in obstacles, and concave-up valves are the least resist­ ant to entrainment, it is not surprising that the convex-up attitude is the norm for shells on river beds and beneath tidal currents . Bivalve mollusc shells appear to undergo frequent changes in attitude as they travel over ripples and dunes, which are bedforms much larger than them­ selves. A valve that is transported convex-up over the upstream side of the bedform is liable to over­ turn on being propelled into the sluggish wake to leeward, with the result that the shell could slide concave-up into and be buried in the trough . Because of their narrow conical form, high-spired gastropods become oriented with the apex upcur­ rent (Fig. IH) . Low-spired and coarsely ornamented forms assume a more random orientation. Cylindri­ cal shells (tentaculitids, orthocones, belemnite guards, articulated crinoid columnals) develop a variety of orientations beneath a current, depending on flow and bed conditions (Fig. 11, J) . Particles of this form tend to roll over the bed, and so develop a flow-transverse biofabric. The fabric changes in­ creasingly towards a flow-parallel one as the shells become rotated into the current direction on meeting obstacles, and as the amount of rotation increases with growing current strength.

229

Fig. 2 Mainly vertically packed and tightly nested shells of Macoma balthica forming a beach deposit in a laboratory wave tank.

Transport in oscillatory (wave) currents

Dispersed shells on smooth beds affected by wave swash and backwash behave much as in one-way flows . Wave action on concentrated bivalve shells forming beaches commonly results in a distinctive biofabric, the valves packing mainly vertically in nests and rosettes (Fig . 2) . In wave-affected shallows, however, where genuinely oscillatory currents exist, field and laboratory experiments point to a different mode of behaviour. The shells either glide (convex­ up if brachiopod or bivalve) or roll over the bed and become orientated so that the long dimension is in most cases parallel with the wave crests (Fig. IK, L) . The combination of oscillatory with steady (e . g . tidal) currents creates more complicated patterns which are as yet little understood. Biofabrics due to organic activity

Some instances of a concave-up attitude assumed by disarticulated bivalve and brachiopod shells found in shallow-marine deposits are with little doubt a consequence of the reworking of the shelly sediment by scavenging organisms, but it is not known how exactly the biofabric arises . Shells dis­ turbed by organisms should possess a random orientation, in contrast to concave-up shells that have settled on the bed in the presence of a current strong enough to swing the particles . References AlIen, J . R. L . 1984 . Experiments on the settling, overturning

230

3 Taphonomy

and entrainment of bivalve shells and related models. Sedimentology 31 , 227-250. Brenchley, P.J. & Newall, G . 1970 . Flume experiments on the orientation and transport of models and shells. Palaeogeography, Palaeoclimatology, Palaeoecology 7,

palaeoclimatology (e .g. Spicer 1981, 1989; Ferguson 1985; Spicer & Greer 1986; Spicer & Wolfe 1987) . Attention here is focused on potential megafossils of terrestrial plants .

1 85 - 220 .

Futterer, E. 1978. Untersuchiingen iiber die Sink- und Transport-geschwindigkeit biogener Hartteile. Neues Jahrbuch fUr Geologie und Paliiontologie, Abhandlungen 155, 318-359 .

Kelling, G . K . & Williams, P.F. 1967. Flume studies of the reorientation of pebbles and shells. Journal of Geology 75, 243- 267.

Kidwell, S . M . , Fiirsich, F.T. & Aigner, T . 1986 . Conceptual framework for the analysis and classification of fossil concentrations . Palaios 1, 228- 238 . Nagle, J . S . 1967. Wave and current orientation of shells . Journal of Sedimentary Petrology 37, 1124 - 1 138. Salazar-Jimenez, A., Frey, R.W. & Howard, J.D. 1982. Concavity orientations of bivalve shells in estuarine and nearshore shelf sediments, Georgia . Journal of Sedimentary Petrology 52, 565 - 586 .

3 . 4 . 2 Plant Material R . A . S PI C E R

Introduction

Allochthonous plant fossil assemblages usually re­ present variously degraded fragmented parts of dif­ ferent individuals and species that lived at varying distances from their ultimate site of deposition and burial. Individual plants are composed of, and pro­ duce, an indeterminate number of organs. Whole plants are almost never found in the fossil record, so palaeobotanical systematics has to handle isolated organs (Spicer & Thomas 1986; Section 5 . 1 .3) that have greatly differing potentials for transport, deposition, and preservation. The interaction of a detached plant organ (or organ fragment) with a fluid medium is governed by its density in relation to that of the fluid medium, together with its shape, size, and surface character­ istics . The transportability of a plant part is largely a function of its terminal fall velocity. Many plant parts are flexible planar objects containing air spaces (e . g . leaves) and their hydrodynamic properties are difficult to model theoretically . Empirical ap­ proaches have proved more successful. Leaves have received most taphonomic attention because of their abundance and utility in biostratigraphy and

Organ dispersal by wind

Aerial transport determines what organ sample a river or lake, for example, receives and therefore 'sees' of the surrounding vegetation . Factors affect­ ing fall velocity in still air include :

Leaf weight. Weight per unit area at abscision is the most critical intrinsic property of a leaf that affects 'flight' and ground dispersal (Spicer 1981 ; Ferguson 1985) . Evergreen taxa typically are heavier and have higher settling velocities .

Leaf shape. Leaf shape has a n effect on fall velocity but shapes with major axes of markedly different length (long and narrow) tend to rotate about the longer axis; such behaviour slightly increases fall time and therefore the chance of greater dispersion from the source (Ferguson 1985) . Leaf size. Although not obviously correlated with fall rate, leaf size affects movement through the branch and trunk space within a forest. Large leaves tend to encounter static obstacles more frequently than small leaves, and any such event either traps the leaf directly, or affects its fall rate . Ferguson (1985) noted a weak positive correlation between leaf size and weight per unit area. Such a correlation would tend to favour the transport of smaller leaves. However, while this may be true for a tree crown as a whole, 'sun' leaves at the top of a tree tend to be smaller but have a higher weight per unit area. Long-distance dispersal of these leaves (and result­ ing preservational bias) is a function of their ex­ posure to high wind energies and their initial height from the ground (Spicer 1981 ) .

Petiole effects. The petiole rarely exceeds 20% of total leaf weight, and even large petioles have negli­ gible effect on fall rate .

Dispersion resulting from air fall. Aerial dispersal of leaves away from a source follows a negative ex­ ponential model (Rau 1976; Spicer 1981) . Rau, in a study of litter deposition in an open lake, used the following equation: Zx = Zr exp

(-k[r-x]),

3 . 4 Transport

Hydrodynamics

where x distance from the lake centre, Zx deposition occurring at distance x, r distance from the lake centre to the shoreline, Zr deposition 1 at the shoreline, and k = - ( r - x ) - l In(Zx Zr- ) . Under some circumstances estimates o f ancient litter productivity may be obtained from the fossil record . =

Water absorption by leaves is governed by the thickness of cuticle and of epicuticular wax, abun­ dance of stomata and/or hydathodes, lamina or petiole damage, water temperature and chemistry, and to a lesser extent by leaf anatomy (Spicer 1981; Ferguson 1985) . Floating times range from several hours to several weeks (Fig. 1); thin chartaceous leaves tend to sink earlier than thick coriaceous leaves (Spicer 1981; Ferguson 1985) . Intact com­ pound leaves float longer than their individual leaflets . Dispersed fruits and seeds (diaspores) exhibit a greater range of floating times than do leaves (e . g . Collinson 1983) . Floating times d o not appear t o be directly related to diaspore size or to the habit of the parent plant (Collinson 1983) . Wood, and in particular logs, can remain afloat for several years and potentially therefore the only hindrance to log dispersal downstream from the growing site is water (channel) depth and in stream obstacles .

=

=

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Post-descent dispersion over the ground. Leaves blown along the ground are distributed laterally by a com­ bination of saltation and rolling. In laboratory ex­ periments the greatest dispersion was found with circular shapes that tended to roll (Spicer 1981) . Dispersion is little affected by leaf size but, as with fall velocities, weight per unit area did prove impor­ tant with light leaves travelling the furthest. Dry curled leaves are easily transported, but wet leaves tend to stick together and suffer minimal ground dispersion. Field experiments (Ferguson 1985) show that most woodland leaves are never disseminated very far from the parent trees (although dispersion is greater in open sites) and that, barring flooding or volcanic activity, even the tallest temperate trees must be growing within 50 m of a body of water to stand any chance of becoming fossilized .

Transport in the water column . Progressive plant tissue saturation follows an 's' shaped curve and does not cease until long after the object has sunk (Greer, unpublished data) . Progressive post-sinking water absorption continues to affect the submerged density of the object, and therefore its behaviour during transport in the water column, until full saturation is reached . When and where the object eventually settles is determined mostly by sub­ merged density and shape, two factors important in determining settling velocity and entrainment be­ haviour. In an aquatic environment plant debris is degraded by biological and mechanical agents, both of which affect the hydrodynamic properties but which produce characteristic degradation patterns seen in fossil material (Spicer 1981, 1989; Ferguson 1985) .

Water transport

Floating. Immediately upon landing on water, plant material absorbs water and soluble substances begin to be leached out. Initially a dry leaf will float and may remain buoyed up by surface tension for sev­ eral weeks, provided that only the bottom surface of the leaf is wetted and the water surface is calm (Spicer 1981) . Plant material could be transported long distances this way, but such conditions are likely to pertain only in slow-flowing rivers pro­ tected from wind (i . e . subcanopy streams), situ­ ations in which long-distance transport is unlikely to occur. 1 00 00 c

Fig. 1 Floating times for freshly abscised leaves of coriaceous evergreen Rhododendron, chartaceous deciduous Fagus sylvatica (abscised dry and brown), and Alnus glutinosa (abscised moist and green) . The leaves were placed in mildly agitated water at room temperature. (Data from Spicer 1981 . )

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232

3 Taphonomy

Settling (fall) velocity in water. In spite of their irregular two-dimensional shape, angiosperm leaves exhibit within-taxon uniformity of settling velocities, as do the more prismatic shapes of coni­ fer needles (Spicer & Greer 1986) . Even irregularly shaped fern pinnules and moss leafy shoots have settling velocities that fall within narrow, moder­ ately well defined, limits . Statistically there is no significant difference between the settling velocities of different broad-leaved taxa (including Ginkgo and fern pinnules), but significant differences do exist between conifer needles and broad-leaved taxa, and between individual conifer taxa (Greer, unpublished data) . In general, conifer needles have a higher settling velocity (e . g . 3 . 03 cm/s for Picea pungens at full saturation) than angiosperm leaves (e . g . 1 . 5 cm/s for Fagus sylvatica at full saturation) . Individual leaves of other broad-lamina taxa such as Ginkgo biloba, however, exhibit fall velocities as high as 6 . 7 crn/s when petiole and lamina configur­ ation produce a hydrodynamically efficient shape that results in a stable gliding fall. Hydraulic sorting, primarily related to settling velocities, has been observed in both low and high energy fluviolacus­ trine delta systems and modelled in relation to spatial and temporal pattern in the source vegetation (Spicer 1981 ; Spicer & Wolfe 1987) . Entrainment. For any given flow, particles concen­ trated near the stream bed are mostly those with the greatest settling velocity. The heaviest particles are transported as bedload and are only in suspension for brief periods of time . As current flow wanes, the lighter fractions progressively settle out. Con­ versely, increases in current flow progressively en­ train material. Flow rate in natural streams and rivers is rarely constant and plant debris is likely to undergo several cycles of deposition and entrain­ ment before permanent burial takes place . Leaf aspect and orientation to fluid flow influence entrainment. Curved leaves, or planar particles in­ clined with their raised edge facing into the flow, are entrained at lower flow rates than those lying flat on the stream bed or inclined with their raised edge pointing downstream . Bed roughness, including bedforms, affects plant particle entrainment (Spicer & Greer 1986) . If bed­ forms (e . g . ripples) are large enough for the plant particles to settle between, the particles are protected from entrainment and often buried rapidly by bed­ form migration . Larger particles pass through the system. Thus, if ripples are noted in a fossil deposit, and only conifer needles are preserved, it cannot be

assumed that angiosperms were not present (even in large numbers) within the source vegetation: they may have been deposited elsewhere because they were too large to be trapped between the ripples . References Collinson, M . E . 1983. Accumulations of fruits and seeds in three small sedimentary environments in southern England and their palaeoecological implications. Annals of Botany 52, 583 - 592. Ferguson, D.K. 1985 . The origin of leaf assemblages new light on an old problem. Review of Paleobotany and Palynology 46, 1 17- 144. Rau, G . H . 1976 . Dispersal of terrestrial plant litter into a subalpine lake . Oikos 27, 153- 160. Spicer, R.A. 1981 . The sorting and deposition of allochthonous plant material in a modern environment at Silwood Lake, Silwood Park, Berkshire, England . US Geological Survey Professional Paper No. 1 143. Spicer, R.A. 1989 . The formation and interpretation of plant fossil assemblages . Advances in Botanical Research 1 6 ,

95- 19 1 .

Spicer, R . A . & Greer, A . G . 1986. Plant taphonomy i n fluvial and lacustrine systems. In: T.W. Broadhead (ed . ) Land plants . pp. 27-44. University of Tennessee Department of Geological Sciences Studies in Geology No. 15. Spicer, R.A. & Thomas, B . A . (eds) 1986. Systematic and taxo­ nomic approaches in palaeobotany. Systematics Association Special Volume 31 . Oxford University Press, Oxford. Spicer, R.A. & Wolfe, ].A. 1987. Plant taphonomy of late Holocene deposits in Trinity (Clair Engle) Lake, northern California. Paleobiology 13, 227-245.

3 . 4 . 3 B ones A . K . BEHRENSMEYER

Introduction

After death, vertebrate skeletons interact with bio­ logical, physical, and chemical processes at or near the Earth's surface . These processes determine whether the bones are destroyed (i. e . recycled) or fossilized. Transport is one of the important pro­ cesses that can affect bones prior to fossilization. Both physical and biological mechanisms of trans­ port may alter life associations of organisms by carrying bones away from the original environment and by mixing taxa from different habitats and time

3 . 4 Transport periods . Such processes also cause abrasion and other types of damage, as well as sorting and differ­ ential preservation of body parts (see also Section 3.3). Biological transport

Biological mechanisms of transport include pred­ ators and scavengers that derive some benefit from collecting bones. One notable modern bone collec­ tor is the African hyaena (Crocuta crocuta); other mammals such as canids, felids, humans, elephants, porcupines, and pack rats also transport bones or parts of carcasses (Shipman 1981) . Predatory birds carry off carcasses and leave accumulations of bones of small vertebrates as regurgitated pellets or debris below a favoured perch . Various small mammalian carnivores leave concentrations of bones in their faeces . Harvester ants (Messor barbarus) also collect bones of small vertebrates and transport them un­ derground (Shipman 1981) . Trampling causes bones to move outward from disintegrating carcasses (Hill 1979) . Fossil accumulations in preserved burrows and cave deposits attest to the bone-transporting activi­ ties of ancient species . It is likely that the fossil record includes examples of biological bone­ transporting processes for which there are no mod­ ern analogues . The Phanerozoic history of such processes and their effect on the vertebrate fossil record is not yet known . Physical transport

Physical processes causing bone transport include water currents and wave action, wind, and gravity. Unfossilized bones are relatively light, with high surface area to volume ratios and irregular shapes, all of which make them readily transportable by moving water. Although bone mineral (hydroxy­ apatite) has a density of about 3 . 2, bones themselves have densities varying from less than 1 .0 (i. e . they float) to 1 . 7 (Behren smeyer 1975) . This is because pore spaces and organic components make up a significant percentage of a fresh bone . Pores may retain air or other gases and keep bones relatively buoyant for hours to days (Behrensmeyer 1975) . Weathered bones that have lost their organic ma­ terial and become cracked are less buoyant. Currents of 20- 30 cm/s can move bones of small to medium­ size vertebrates (e .g. rodent to sheep) but stronger currents are required for bones of larger animals (e . g . cow, elephant) . Teeth have densities ap-

Hydrodynamics

233

proaching 2.0 and almost always require stronger currents for transport than do bones, regardless of the size of the animal. Experiments in natural rivers with flood velocities of 1 .0 m/s demonstrate that bones can be transported a kilometre or more in a single year. The hydrodynamic behaviour of bones can be predicted to some extent by considering them as sedimentary particles and calculating their 'quartz­ equivalents' . This is the size of a quartz grain with a settling velocity equal to that of the bone, and it can be calculated based on measurements of actual set­ tling velocities of bones in water (Behrensmeyer 1975; Shipman 1981) . Bones and teeth of approxi­ mately equal sizes can have very different quartz­ equivalents (Fig. 1 ) . Those with smaller equivalent quartz grains are generally more transportable, although shape and orientation to a current can cause exceptions to this rule . Scapulae are small and light relative to other bones in a skeleton, but their shape is also streamlined so that they are less easily moved than an equivalent quartz sphere . In fossil deposits, the difference in grain size of matrix sediment and bone has been used to assess transport history (Shipman 1981) . If bones are pre­ served with grains of near-equal quartz diameters, this is interpreted as an indication that the bones were transported and hydraulically sorted. In con­ trast, if bones are associated with sediment of much finer quartz-equivalents, then minimal transport is inferred . Since the relationship between transport and quartz-equivalents can be influenced by in­ dividual bone shapes, considerable caution is necessary in such interpretations . Moreover, the grain sizes that are available for transport, rather than hydraulic sorting, can control which quartz­ equivalents are associated with bones at the time of burial.

Sorting. Differing hydrodynamic behaviour of bones in a single skeleton results in sorting (separation of body parts according to transport rates) and win­ nowing (removal of the lighter elements, leaving a 'lag' of the heavier, less transportable bones) . Experi­ ments in flumes and natural rivers have demon­ strated that there are three distinct transport groups ('Voorhies Groups') for medium to large mammals (in order of decreasing mobility) : Group I vertebrae, ribs, sternum; Group 11 - limb parts; Group III - skulls, mandibles, teeth (Voorhies 1969; Behrensmeyer 1975; Shipman 1981) . Bones from a single point source (i. e . a skeleton) show progressive sorting with continued current action. Distinct pat-

3 Taphonomy

234 26.9

mm

8.6 mm

14.8

mm

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3.1

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S h eep m o l a r Ast raga l u s m ed i u m artiodactyl

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( Hylochoerus)

H o rse m o l a r

terns of sorting in a fossil deposit thus indicate the interaction of currents with a localized bone source . Input from multiple sources of bones along natural rivers or beaches obscures patterns of sorting for individual carcasses . If there are many point sources of bones, all body parts (from different individuals) can co-occur in deposits formed by water currents (Hanson 1980) . Bones of small vertebrates also can be moved by wind action on beaches, dune fields, and ephemeral river beds. Dust-devils are effective mechanisms for transporting and scattering small bones in arid en­ vironments . Gravity assists in bone movements on steep slopes, as in caves and sinkholes . The low density of bones helps to keep them near the surface and exposed to slope wash and mass move­ ments of sediment.

Orientation . The orientations of individual bones indicate the influence of hydraulic processes on the bone assemblage (see also Section 3.4. 1 ) . In strong currents, elongate bones generally orient parallel to the flow direction, with the heavier end upstream . In shallow water or in weak currents, such bones may orient perpendicular to the current and roll downstream around their long axis (Voorhies 1969; Behrensmeyer 1975; Shipman 1981) . Determining flow direction from bone orientations must take both of these patterns into account. Large bones may act as 'traps' for smaller ones, which accumulate against the upstream side or in the downstream zone of flow separation (shadow) . The orientation of the larger bones may influence those of associated smaller ones.

D e r m a l s c u te

(Crocodylus)

Fig. 1 The hydraulic equivalents of examples of Recent bones, as determined by their settling velocities and calculations of the diameter of a quartz sphere that would settle at the same velocity. Bones and quartz grains are drawn to the correct relative sizes. (After Behrensmeyer 1975; reproduced with permission from the Museum of Comparative Zoology, Harvard University. )

Concentration . Dense concentrations of fossil bones in river deposits are often attributed to hydraulic processes. However, experiments in modern rivers indicate that fresh bones are generally too light to form permanent patches or 'bone bars' unless there is a point source nearby and/or an obstruction that causes transport to cease abruptly . Repeated win­ nowing and reworking can concentrate denser elements (e.g. teeth) as part of the gravel 'lag' deposit in fluvial sediments . Previously fossilized bones with higher densities may be incorporated into such lags, mixing remains from periods of 100 10 000 or more years to create a time-averaged sample of the original vertebrate communities (Behrensmeyer 1984) . Abrasion . Hydraulic transport can abrade and break bones, but experiments in tumbling machines and in natural rivers indicate that it takes considerable bone - sediment interaction to cause significant damage to fresh bones and teeth (see also Section 3 . 1 ) . Weathered bones are more vulnerable to abra­ sion and breakage in transport situations . Fresh experimental bones can travel over 3 km in a sand­ and gravel-bed river with only minor loss of surface detail due to abrasion. Exposure to poorly sorted sand for up to 35 h in a tumbling machine is necess­ ary to produce gross changes in fresh bones. Fossil dinosaur and crocodile teeth subjected to the equivalent of 360 -480 km of transport in a tumbling machine with coarse sand showed negligible dam­ age to enamel surfaces (Argast et al. 1987) . Thus, bones and teeth can experience considerable trans-

3 . 5 Fossil Concentrations

235

port without showing significant abrasion. Con­ versely, stationary bones may be 'sand-blasted' by water or wind-borne sediment and heavily abraded without significant transport. Thus, it is very dif­ ficult to judge the transport history of a bone from its appearance .

thus contain evidence of vertebrate palaeoecology for areas and time periods that often are not directly comparable with samples of vertebrate communi­ ties from modern ecosystems.

Burial. The same physical processes that transport bones also bury them. In channels and on beaches, bones are buried and exhumed many times prior to destruction or fossilization as they move along with bedload sediment. They may be overtaken by mov­ ing bedforms (ripples, sand waves), and scour on their downstream sides also promotes burial. Per­ manent burial happens when the bone is removed from the active zone of sediment transport; this can occur when the channel abandons its course or when unusual flood conditions alter its bottom morphology . The taphonomic history of bones should be ana­ lysed prior to ecological interpretations of species represented in a vertebrate fossil assemblage be­ cause they are readily transported by both physical and biological processes . The tendency for bones to be buried and reworked repeatedly in fluvial and shoreline environments also implies that trans­ ported remains may represent a substantial amount of time-averaging. Transported bone assemblages

Argast, 5 . , Farlow, J . O . , Gabet, R.M. & Brinkman, D . L . 1987. Transport-induced abrasion of fossil reptilian teeth : impli­ cations for the existence of Tertiary dinosaurs in the Hell Creek Formation, Montana . Geology 15 , 927-930. Behrensmeyer, A.K. 1975 . The taphonomy and palaeoecology of Plio-Pleistocene vertebrate assemblages east of Lake Rudolf, Kenya . Bulletin of the Museum of Comparative Zoology 146, 473- 578 . Behrensmeyer, A.K. 1984. Taphonomy and the fossil record . American Scientist 72, 558 - 566. Hanson, C.B. 1980 . Fluvial taphonomic processes: models and experiments . In: A. Behrensmeyer & A. Hill (eds) Fossils in the making, pp. 156 - 1 8 1 . University of Chicago Press, Chicago. Hill, A. 1979 . Disarticulation and scattering of mammal skel­ etons . Paleobiology 5, 261 -274 . Shipman, P. 1981 . Life history of a fossil. Harvard University Press, Cambridge. Voorhies, M.R. 1969 . Taphonomy and population dynamics of an early Pliocene vertebrate fauna, Knox County, Nebraska. University of Wyoming, Contributions to Geology

References

1,

1 - 69.

3 . 5 Fossil Concentrations and Life and Death Assemblages F . T . FURSICH

Fossil concentrations

A fossil concentration is defined as any relatively dense accumulation of fossils, irrespective of taxo­ nomic compOSition, state of preservation, or degree of post mortem modification. Fossil concentrations are nearly exclusively accumulations of hard parts. They are therefore regarded here as synonymous with skeletal concentrations of fossil organisms (Kidwell et al. 1986) . As the size of the biogenic hard parts is not restricted, this definition includes dinosaur bone beds as well as coral reefs, shell beds of bivalves and those of ostracodes (see also Section 3.4) .

Fossil concentrations also include several types of Fossil-Lagerstatten, especially those formed by rapid burial or by condensation (Section 3 . 6) .

Descriptive classification. Fossil concentrations can be described in several ways, stressing either taxo­ nomic composition, bioclastic fabric (degree of packing), geometry, or the internal structure of the deposit (Fig . 1 ) . Each of these aspects carries some genetic significance . The taxonomic composition largely depends on the ecology of the component taxa and, to a lesser degree, on the hydrodynamics of their accumulation . The biofabric, that is the three­ dimensional arrangement of skeletal elements in

236

3 Taphonomy

TAXO N O M I C COMPOS I T I O N

G E O M ETRY

PAC K I N G _

m o n otyp i c

-: matrix s u p po rted

po lyty p i c

b i oclast - s u p p o rted

-

-

stringer pave m e n t pod clump lens wedge bed

I NT E R N A L STRUCTU R E S I MPLE C O M P L EX

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Fig. 1 Major features used in the descriptive classification of fossil concentrations and their genetic significance. Shaded box predominant; white box rare. (After Kidwell et al. 1986 . )

1-----+--4L .--t--JJ-----I--.------I ECOLOGY

HYDRODY­ NAM I CS

TOPOG RA P H Y

the matrix, includes skeletal orientation, degree of packing, and sorting by size and shape . The bio­ fabric is strongly influenced by hydrodynamic con­ ditions, whilst ecology and compaction may be additional factors . The geometry of a fossil concen­ tration depends on the pre-existing topography of the depositional surface (e .g. burrow fills), the ecol­ ogy of the hard part producers (e .g. clumps of mussels) and other organisms (e .g. shell-lined bur­ rows), and on the hydrodynamic conditions which, at the time of hard part concentration, produce a topography (e . g . by the migration of ripples, exca­ vation of scours, etc . ) . The internal structure provides information on the ecological and hydrodynamic history of the deposit. Simple (i . e . internally homo­ geneous or, at the most, with unidirectional trends) and complex skeletal concentrations can be dis­ tinguished . In the latter, features such as grain size, degree of articulation, and orientation vary in a complicated pattern .

Genetic classification . Fossil concentrations can also be classified genetically, based on the main concen­ trating processes . The formation of concentrations is governed by the interplay of net rate of sedi­ mentation, net rate of production of biogenic hard parts, and to a lesser extent diagenetic processes . Ac­ cordingly, biogenic, sedimentological, and diagen­ etic concentrations can be distinguished (Fig. 2) . Biogenic concentrations result from the gregarious behaviour of organisms with hard parts (e .g. mussel beds) or of organisms which concentrate skeletal elements (e . g . during the feeding process) . Sedimen­ tological concentrations are produced by hydraulic processes which may represent short-term events (e . g . storms) or long-term processes (e . g . back­ ground current and wave action) . Examples include shelly storm lags or condensed shell beds . Diagenetic concentrations are the result of post-burial physical

ECO LOG I CAL & H Y D RODYNAM I C H I STORY

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. . . . ·.·...

·a.Q '

.

.

.

.

'

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Fig. 2 Genetic types of fossil concentrations based on biogenic, sedimentological, and diagenetic processes . White area of the triangle represents concentrations of mixed origin. The longer the time-span involved in the formation of a concentration, the more likely it will be mixed in origin. (After Kidwell et al. 1986 . )

or chemical processes, including compaction as well as selective pressure solution of matrix in bioclastic limestones . These processes act in most fossiliferous sediments, but are rarely as significant as biogenic or sedimentological processes . Most fossil concentrations are formed by more than one process. For example, a storm-reworked mussel bed is of mixed biogenic and se dim en to­ logical origin; a strongly compacted layer of bivalves killed by drastic changes of salinity represents a diagenetically enhanced biogenic concentration.

237

3 . 5 Fossil Concentrations Of particular importance for the formation of fossil concentrations is the combination of low net rates of sedimentation with high net rates of bio­ genic hard part production. Zero net rates of sedi­ mentation (i. e . omission) and negative net rates (corresponding to erosion) result in different types of fossil concentrations which frequently exhibit sharp lower or upper contacts (Kidwell 1986) . When subsequently undisturbed, such concentrations and their bed contacts can be interpreted very pre­ cisely. In reality, however, the contacts are com­ monly modified by burrowing organisms and/or diagenesis .

Geological and palaeontological significance. Fossil concentrations are a useful tool in basin analysis, furnishing information on bathymetry, rate of sedi­ mentation, hydrodynamic regime, and environmen­ tal gradients . The prevalence of particular types of concentration, such as those produced by storms, and their frequency through time allow inferences about basin configuration and evolution. Along onshore - offshore gradients for example, sedimen­ tological concentrations which dominate in shallow, nearshore environments are gradually replaced by biological concentrations in deeper shelf areas . Among sedimentological concentrations those exhibiting wave influence are most prominent in very shallow water, those of storm origin in shallow to intermediate shelf depths, whilst in lower shelf regions sediment starvation and condensation are the governing factors . Biostratinomic features of the skeletal elements such as biofabric, articulation, sorting, fragmen­ tation, abrasion, bioerosion, and encrustation pro­ vide additional data on residence time on the sea floor, wave versus current influence, degree of re­ working, and sediment starvation (see also Section 3.3). The palaeontological significance of fossil concen­ trations varies greatly depending on their genesis (see below) .

Life and death assemblages

Definitions. The term assemblage has several mean­ ings (Fagerstrom 1964) . According to some authors, assemblages consist of organisms derived from more than one community (i . e . they exhibit signs of mixing) . In another, broader definition adopted here, the term refers to any group of organisms

from a geographical locality. A life assemblage accord­ ingly is defined as any group of living organisms from a geographical locality . It may represent a whole community or only parts of it. A death assem­ blage ( thanatocoenosis) consists of the preserved elements of a life assemblage after its death and decay. As a rule, soft-bodied organisms are no longer represented in a thanatocoenosis . The species diversity of a thanatocoenosis is therefore much lower than that of the life assemblage . The trophic composition of a living community is commonly not adequately reflected in the thanatocoenosis . The term taphocoenosis ( allochthonous thanatocoenosis of some authors) refers to hard parts of organ­ isms which became embedded together after having been subject to biostratinomic processes such as sorting, admixture of shells from adjacent habitats or from stratigraphically older units, mixture of skeletal elements resulting from time-averaging, or selective destruction by physical, chemical, or bio­ logical agents . A fossil assemblage differs from a taphocoenosis in that post-burial diagenetic pro­ cesses have been operating which led to lithification or partial destruction of the hard parts . In cases where biostratinomic and diagenetic pro­ cesses did not play a significant role, the fossil assemblage will be roughly identical to the thanato­ coenosis . The terms taphocoenosis and thanatoco­ enosis are often used as synonyms . In the definition given here they do, however, characterize different stages of the transition of a life assemblage to a fossil assemblage (Fig. 3) . =

=

Time averaging. The quality of a taphocoenosis (and thus often of the resulting fossil assemblage) largely depends on the time factor. Rapid in situ burial of a life assemblage (e .g. during storms) may produce a taphocoenosis which faithfully records species composition and age structure of the organisms with hard parts . Under normal circumstances, how­ ever, taphocoenoses represent time-averaged relics of life assemblages . Time-averaging refers t o the mixing o f skeletal elements of non-contemporaneous populations or communities . This telescoping of biological data representing tens, hundreds, or even thousands of years into a single geological time plane drastically alters the quality of the data. Short-term fluctuations in species composition and in the morphological range of species, reflecting variations in salinity, oxygen, or other environmental factors, cannot be recognized from time-averaged assemblages . The occasional dominance of opportunistic species in a

3 Taphonomy

238 L I F E AS S E M B LAG E

THANATO C O E N O S I S

TA P H O C O E N O S I S

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community will be considerably tuned down in time-averaged relics . Species richness and often also evenness in such taphocoenoses will be greater than that of the living communities (excluding soft­ bodied organisms) from which they are derived (Fig. 4) . Some attributes of live communities, such as trophic structure and taxonomic composition, stand a better chance of being preserved during time-averaging than others (e .g. numerical abun­ dance) (Staff et al. 1986) . Even very short time­ averaging (e .g. 10-20 years) can produce significant differences between living communities and tap ho­ coenoses . For example, organisms living during different stages of community succession will in­ variably become mixed after death . Similarly, new taxa are introduced into the taphocoenoses by tapho­ nomic feedback, i.e . the spectrum of live - dead interactions . In this case, biostratinomic processes need not be involved .

Palaeontological significance. Time-averaged tapho­ coenoses have therefore a different quality than living communities and the two cannot be strictly compared . On the other hand, time-averaged tapho­ coenoses often record the large-scale environmental conditions more faithfully and thus may be more indicative of long-term trends than living communi­ ties. Several studies (e . g . Warme 1971) have de­ monstrated that taphocoenoses do reflect the broad environmental framework and give an, albeit rough, account of the dominant taxa with hard parts liv­ ing in and characteristic of these environments . The fidelity of taphocoenoses and resulting fossil as­ semblages for palaeoecological analysis thus largely depends on the degree of biostratinomic and dia­ genetic distortion, the degree of time-averaging, and on the frequency and degree of environmental fluctuations .

== -==- � -� 'I

b

c

A

a

·Ih ==-===-=-.�

d

a

B

Fig. 4 . Effects of time-averaging on species diversity: a, b , c, d, communities; and 1 , 2,3, different species of a community. Shaded areas represent slices of time . A, Time­ averaging substantially increases both evenness and species richness . B, The dominance of an opportunistic species (stippled) is tuned down in a time-averaged sample . Similar changes take place in other community characters, such as trophic composition and composition of life habits.

References Fagerstrom, J.A. 1964. Fossil communities in paleo­ ecology. Bulletin of the Geological Society of America 75, 1197- 1216.

Kidwell, S.M. 1986 . Models for fossil concentrations: paleo­ biologic implications. Paleobiology 12, 6 - 24. Kidwell, S.M., Fiirsich, F.T. & Aigner, T . 1986 . Conceptual framework for the analysis and classification of fossil concentrations . Palaios 1, 228 - 238.

3 . 6 Obrution Deposits Staff, G . M . , Stanton, R.J., Jr. , Powell, E.N. & Cummins, H. 1986 . Time-averaging, taphonomy, and their impact on paleocommunity reconstruction: death assemblages in Texas bays . Bulletin of the Geological Society of America 97,

239

Warme, J . E . 1971 . Paleoecological aspects of a modern coastal lagoon. University of California Publications in the Geological Sciences 87, 1 - 131 .

428 - 443 .

3 . 6 Obrution Deposits C . E . BRETT

General characteristics

The term obrution refers to fossil assemblages pre­ served by very rapid burial of intact organisms and is approximately equivalent to 'smothered bot­ tom assemblages' (Seilacher et al. 1985) . Obrution deposits are generally considered to represent one endmember of extraordinarily preserved biotas, or conservation Lagerstatten (Seilacher et al. 1985); in contrast, stagnation deposits are produced by depo­ sition of organic remains in anoxic environments (see also Section 3 . 1 1 . 1) . However, decay of organic matter is exceptionally rapid (days to months) even in anaerobic environments (Section 3 . 1) . Weak cur­ rents, which appear to be present even in black shale depositional settings, will then cause complete disarticulation and scattering of skeletal elements . Hence, rather than being a distinct endmember, obrution is involved in most, if not all, examples of exceptionally preserved, articulated fossils . Examples of obrutionary Lagerstatten (Seilacher et al. 1985) include the famous echinoderm occur­ rences, such as the Mississippian Crawfordsville crinoid beds of Indiana or the Jurassic Gmiind horizon of southern Germany. Undoubtedly, many of the classic soft-bodied fossil Lagerstatten, such as the Cambrian Burgess Shale (Section 3 . 1 1 . 2), the Devonian Hunsriick Slate (Section 3 . 1 1 .4), and the Jurassic Solnhofen Lithographic Limestones (Section 3 . 1 1 . 7), represent obrutionary stagnation deposits . Here the combination of rapid burial and anoxia facilitated preservation of soft tissues. Taphonomic and sedimentological aspects

Obrution deposits are recognizable primarily from taphonomic aspects of their enclosed fossils . Preser­ vation of completely articulated multielement skel­ etons in trilobites, echinoderms (Figs 1 - 3), and

vertebrates normally requires rapid entombment. In addition, other sedimentological evidence may indicate rapid emplacement of sediment layers . Each obrution deposit consists of two basic com­ ponents: the buried horizon itself (smothered layer) and the burial layer (Fig. 2) . The buried horizon represents a former sediment-water interface, and consequently may display a variety of features that indicate a span of non-deposition prior to final burial. The most obvious examples are obrution deposits associated with hardgrounds, in which the buried layer is an encrusted and bored pavement. Remains of the last community to inhabit the hard substrate may be extraordinarily well preserved, as in cases of complete edrioasteroids, cystoids, and crinoids remaining attached to hardgrounds (e .g. in the Middle Ordovician of Ontario; Brett & Liddell 1978) . Where the buried horizon consisted of uncon­ solidated sediment, it may be recognizable as a concentrate or lag of shells, bones, or other skeletal elements, abruptly overlain by less fossiliferous or even barren sediments (Fig . 2) . If such a skeletal lag is absent, buried horizons may be extremely cryptic. Well preserved remains of sessile or semisessile organisms may occur directly on the buried surface, while skeletons of infaunal organisms may be pre­ served directly beneath it in their original burrows . In certain obrutionary layers there is also evidence of physical disturbance of the benthic environment shortly before sediment deposition: for example, shells with fragile encrusting epibionts may occur in inverted positions . This demonstrates that the shells were flipped, in some cases to concave upward positions, shortly before they were buried (Fig. 1C) . Skeletal remains on the buried horizon may be concentrated into windrows, aligned, or otherwise preferentially reoriented by the agent of final burial. Such features of these horizons may give clues as to the strength and direction of currents associated

240

3 Taphonomy

Fig. 1 Biostratinomic features associated with an obrutionary echinoderm Lagerstatte; Lower Rochester Shale, Homocrinus beds, Lockport, Niagara County, New York. Figs A, B, D, x 2; Fig . C, x 3. A,B, Articulated specimens of the crinoid Asaphocrinus ornatlls. A, Crinoid attached by its original holdfast to a brachiopod; note shell pavement of buried horizon . B, Specimen displaying incipient disarticulation; note staggering of individual segments which indicates that the crinoid had undergone some decay prior to burial. C, Edrioasteroid HemiClJstites parasiticlIs attached to the fold of a Striispirifer brachiopod valve; spe­ cimen is on the undersurface of a shale bed - hence it must have been overturned shortly before burial. D, Ophiuroid Protaster stellifer, in possible crawling position; specimen is in sparsely fossiliferous mudstone overlying buried horizon and probably represents a failed escape attempt.

with the burial event (see also Section 3 . 4 . 1 ) . Rarely, fossils in obrution deposits have been transported considerable distances from their living sites, as in the case of trilobites (Triarthrus) with preserved appendages from the Ordovician Frankfort Shale of New York, that occur within turbidites (Cisne 1973) . Fossils in the famous Solnhofen Limestone show evidence for abrupt importation into an anoxic, probably hypersaline basin or lagoon; some organ­ isms apparently were alive at the time, as indicated by evidence of a 'death struggle' (Seilacher et al. 1985; Section 3 . 1 1 . 7) . The burial layer consists o f an interval o f sediment overlying the smothered horizon, which was rapidly deposited, normally in a period of a few hours to a few days . It is typically unfossiliferous or sparse­ ly fossiliferous, and may display features such as fining-upward size grading, and planar and cross lamination indicative of deposition from a waning current . Most commonly the burial layer consists of barren structureless mud stone or siltstone . If escape burrows or delicate articulated skeletons extend up­ ward into this layer, it may be possible to deter­ mine the approximate thickness (with corrections for compaction) and rate of deposition of the burial sediment. Geological agents that contribute to obrution de­ posits include turbidity currents, grain or debris flows, and, especially, major storms and the accompa­ nying flood runoff. In many cases, fine-grained sediments, resuspended in shallow waters by storm waves, may be carried by gradient or turbidity flows into offshore areas, where they accumulate rapidly. Burial layers may consist of relatively coarse-grained sediment, in which case they are readily inter­ preted as rapid accumulations of suspended sedi­ ment loads . However, most of the best obrution Lagerstatten are preserved in and beneath layers of fine-grained sediments, for which extremely rapid sedimentation might seem an impossibility . The very rapid emplacement required for exceptional preservation may occur if muds were flocculated or pelleted. These sediments behave hydrodynami­ cally as silts or even fine sands, rather than muds. Rapid entombment may also occur if the sediment suspensions are extremely dense, as in thick mud slurries . Obrution deposits may be accentuated by early diagenetic mineralization (Fig . 2) . For example, fos­ sils may be encapsulated within carbonate con­ cretions, as in the well known Carboniferous Mazon Creek sideritic nodules (Section 3 . 1 1 . 5) . Carbon­ ate precipitation is probably favoured both by in-

3 . 6 Obrution Deposits

RPD

B U R I A L LAY E R

RPD-d i s r u pted

. . . . RPD-stab i l ized

\ Fig. 2 Taphonomic history of an obrutionary deposit with enrolled, pyritized trilobites . Preburial disturbances of sea floor environment (including toxic conditions and/or high turbidity) induces trilobite enrollment. Burial of the sea floor entombs the trilobite and decay of organic matter causes redox potential discontinuity (RPD) to rise above the trilobite and associated tube-dwelling annelid. Local production of reducing sulphidic microenvironments around decaying organisms favours precipitation of iron sulphides at these sites. (After Speyer 1987.)

241

creased pH, as a result of ammonia formation, and bicarbonate concentrations produced as a by-product of bacterial sulphate reduction (Section 3 . 8 . 2) . Fos­ sils within obrution layers commonly display films or external moulds of pyrite (Fig. 2) . This has been interpreted as a result of rapid entombment of or­ ganic nuclei within otherwise organic-poor, anoxic non-sulphidic sediments (Section 3 . 8 . 3) . The Eocene Messel Lake deposits of Germany display soft tis­ sues of bats, birds, and other organisms preserved by siderite-replaced bacteria (Section 3 . 1 1 .8) . Obrutionary deposits are more likely to b e pro­ duced in certain environments than in others . For example, shallow-water environments are con­ ducive to episodic sedimentary events, which might preserve smothered bottom assemblages; however, these will rarely be preserved permanently in en­ vironments above normal wave base, as most will be cannibalized by later erosion. Relatively low­ energy environments, slightly below normal storm wave base, are probably the optimal areas for pres­ ervation of obrution deposits . Obviously, obrution deposits will be more numerous in areas of heavy sedimentation than in regions of relative sediment starvation. However, very large inputs of sediment may have a diluting effect on fossil occurrence, and may inhibit the recognition of obrution deposits . Conversely, obrution layers may be common in condensed sedimentary sequences where they re­ cord the only permanent sediment accumulation. Seilacher et al. (1985) predicted that obrution de­ posits will be best developed in sediments over­ lying the caps of coarsening-upward cycles . Biological aspects of burial

Organisms found in obrution layers may have been killed by asphyxiation due to the burial event itself or by some other agency prior to deposition of the sediment. In many cases there is evidence of pre­ burial disturbance . For example, layers of enrolled trilobites, which in some instances are traceable for several kilometres, appear to record instances in which trilobites were able to respond to environ­ mental stimuli, such as changes in the water tem­ perature, chemistry, or salinity prior to the actual burial event (Speyer 1987; Fig. 2) . Fossils in obrution deposits commonly display evidence that organisms had undergone incipient decay (e .g. minor dis­ articulation and/or displacement of skeletal ossicles) and, therefore, must have died at least several hours before final burial (Figs 18, 3B) . Such 'event separ­ ation' could occur during the course of a single large

242

3 Taphonomy

Fig. 3 Obrutionary deposits with implications for trilobite autecology. A, Large cluster of Phacops rana (Green) from the Middle Devonian of New York; species-specific clusters of this sort suggest gregarious life habits. B, Group of Dechenella rowi showing partial articulation; these specimens underwent minor decay prior to burial . C, Cluster of moult elements (thoracopygidium and cephalon) of Phacops rana . Such specimens indicate that some trilobites moulted in clusters . D, Two specimens of Phacops rana showing differential preservation. Upper specimen shows thin wrinkled cuticle and may represent a soft-shelled individual. All figures x 1 . A, C, D, Windom Shale at Penn Dude Quarry, Blasdell, Erie Co . , New York; B, Wanakah Shale, Lake Erie Shore near Wanakah, Erie Co . , New York. (From Speyer & Brett 1985 . ) (Reproduced with permission from the Lethaia Foundation . )

storm which might cause disturbances in water tem­ perature, salinity, or chemistry during early stages, as well as later influxes of sediment. Specimens of ophiuroids and bivalves may be preserved in burrowing positions within the burial layer, over­ lying smothered benthic assemblages (Fig. 10) . Es­ cape burrows likewise reflect a direct response to

burial, in this case a successful one . Schafer (1972) and Peterson (1985) observed that infaunal bivalves usually move upward and out of their burrows in response to burial . Commonly, they are unable to move upward through the water-rich burial sedi­ ments themselves, and die at the former sediment ­ water interface .

3 . 6 Obrution Deposits The thickness of burial layers required to trap and kill organisms varies not only with the type of organism, but with the grain size, density, and rate of deposition of the burial medium . Echinoderms may be particularly vulnerable to death by burial in that their water vascular system may be easily fouled by fine-grained suspended sediment (Fig. 1 ; Seilacher e t a l . 1985) . Schafer's (1972) seminal studies of preservation processes in the North Sea demon­ strated that ophiuroids can escape from layers of sediment up to 5 cm thick in a matter of minutes, while echinoids can burrow out of substantially thicker layers . Kranz (1974) demonstrated that cer­ tain species of bivalves display differing 'escape potential' ; deep and rapid burrowing forms could commonly escape from substantially thicker lay­ ers than those which were semisessile as adults . Peterson (1985) noted that juvenile bivalves are commonly better able to escape rapid burial because of their lower mass, which allows them to move upward through water-rich burial sediments . Conclusions

The significance of obrution deposits is threefold: palaeobiological, sedimentological, and strati­ graphical. 1 Obrution deposits are the most numerous type of conservation Lagerstatten (Section 3. 1 1 . 1) . As such they provide 'snapshots' of ancient sedimentary environments, with unique opportunities to study detailed morphology of fragile organisms that are not normally preserved intact. They may permit direct observations of certain types of organism ­ substrate associations and rarely, as in the case of clustered trilobites from the Palaeozoic (Fig . 3), they may even permit inference of life behaviours (Speyer & Brett 1985; Speyer 1987) . 2 Obrution deposits are a type of sedimentary event deposit . Thus, they permit recognition of subtle 'mud tempestites', distal turbidites, and other types of event beds . The highly episodic nature of

243

sedimentation, even in seemingly monotonous se­ quences, may be demonstrated by means of closely­ spaced sampling and identification of obrution deposits . Taphonomy of such burial layers may provide important clues as to sedimentary dynamics in fine-grained sedimentary sequences . 3 Some obrution deposits are extremely widespread and, as such, provide a special type of stratigraphic marker. Inasmuch as they can be demonstrated to represent single events, they are probably iso­ chronous over much of their range and display unique taphonomic and palaeontological features that permit their easy identification. Recognition and mapping of obrution deposits may greatly re­ fine stratigraphic correlations in some sedimentary basins. References Brett, C . E . & Liddell, W.D. 1978 . Preservation and palaeo­ ecology of a Middle Ordovician hardground community. Paleobiology 4, 329 - 348 . Brett, C . E . , Speyer, S . E . & Baird, G . c . 1986. Storm-generated sedimentary units: tempestite proximality and event stratification in the Middle Devonian Hamilton Group . Bulletin of the New York State Museum 457, 129- 156. Cisne, J . L . 1973 . Beecher's trilobite bed revisited : ecology of an Ordovician deep water fauna. Postilla 160, 1 - 25. Kranz, P.M. 1974. Anastrophic burial of bivalves and its paleoecologic significance . Journal of Geology 82, 237-265 . Peterson, C . H . 1985 . Patterns of lagoonal bivalve mortality and their paleoecological significance . Paleobiology 11, 139 - 153.

Schafer, W. 1972. Ecology and paleoecology of marine environ­ ments . University of Chicago Press, Chicago . Seilacher, A., Reif, W.E. & Westphal, F. 1985 . Sedimentologi­ cal, ecological, and temporal patterns of fossil Lagerstatten . Philosophical Transactions of the Royal Society of London B311, 5-23.

Speyer, S.E. 1987. Comparative taphonomy and palaeoecol­ ogy of trilobite Lagerstatten. Alcheringa 11, 205 - 232. Speyer, S . E . & Brett, C . E . 1985 . Clustered trilobite assem­ blages in the Middle Devonian Hamilton Group . Lethaia 18, 85 - 103 .

3 . 7 Flattening D . E . G . B RI G G S

3 . 1 1 . 6), for example, the body chamber is fractured in the characteristic manner. By the time the phragmo­ cone was compacted, however, most of the shell mineral had dissolved, and it therefore deformed by wrinkling (Fig . ID) . Compaction of ammonites in the Solnhofen Limestone led to the formation of a collapse caldera and pedestal (Section 3 . 1 1 .7) . The thickness of skeletal material also affects the response to flattening. Thick shells fracture in well defined patterns . Thin-shelled forms (e .g. some brachiopods), however, fracture and imbricate in much more subtle ways; the effects may only be evident in thin section . The relatively thin cuticle of Cambrian olenellid trilobites, and their occurrence in fine-grained lithologies, accounts for the rarity of specimens preserving the original convexity. The bones of vertebrates are also subject to brittle failure .

Introduction

An analysis of the mode of flattening of fossils (including collapse due to decay, and compaction as a result of overburden pressure) is important for the information it reveals about their taphonomic history, and also as a basis for the restoration of the organism to its former three-dimensional appear­ ance . Failure to understand the effects of compaction in different orientations to bedding has sometimes resulted in the establishment of separate taxa based only on preservational variants . Fractures which are due to compaction have, on occasion, been mistaken for the results of predation. The degree and nature of flattening is deter­ mined by a number of factors : (1) the grain size and composition of the sediment (coarser-grained sediments are more resistant to compaction result­ ing from the supporting effect of the grains and the lower pore-water volume); (2) the morphology and mechanical strength of the organism; (3) the orientation of the buried organism to the bedding; (4) the nature and timing of diagenesis; and (5) the infilling of cavities .

A

Hard parts

Mineralized skeletons normally fracture when they are compacted . The pattern which results depends mainly on geometry. Ammonites, for example, are commonly buried with the plane of coiling parallel to bedding. They usually retain their original di­ mensions except in the aperture where the retain­ ing forces of the skeleton are reduced. Compaction is a two-phase process (Seilacher et al . 1976) the body chamber normally collapses before the phragmocone, which is strengthened by the septa (Fig. lE, C). The junction between the body chamber and phragmocone is therefore marked by a pro­ nounced radial fracture . Much of the compaction, however, is accommodated by prominent fractures running alongside the keel, which forms a thick­ ened, strengthening structure . The two phases of collapse are particularly distinct where the shells are subject to dissolution . In the Jurassic Posidonia Shales of Holzmaden, southern Germany (Section

·

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.

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.

.

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.

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-

F

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.

. .... ,

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,-

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.

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.

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Fig. 1 Preservation and flattening of an ammonite, illustrated in diagrammatic section . A, Uncompacted shell preserved in a coarse early-cemented sediment. B, First of two-phase compaction, body chamber only . C, Second phase, phragmocone compacted. D, Delayed compaction of phragmocone (above), and entire shell (below), wrinkling due to decalcification. E, Compaction prevented by concretion formation. F, Body chamber concretion . G, Concretion external to the shell . (After Seilacher et al . 1976.)

244

3 . 7 Flattening Certain shapes are more resistant to compaction than others, and the solid margins of bones tend to be more resistant than the core . Early diagenesis may have a significant influence on compaction. An entire shell or bone may be enclosed in a concretion (Fig. lE) . Alternatively, early diagenetic minerals may form only in the local­ ized reducing environment promoted by organic decay within a cavity (Section 3 . 1) . Sediment in the body chamber of ammonites, for example, may form a concretion, usually of phosphate (Fig . IF) . The chambers of the phragmocone may also resist com­ paction if sediment gains access to them and be­ comes phosphatized, or if they are reinforced by linings of early diagenetic pyrite or drusy calcite (Seilacher et al. 1976) . Concretions may also oc­ casionally form below the shell, retaining an exter­ nal mould where it dissolves (Fig . IG) . Plants

Most plant fossils are preserved as flattened 'com­ pressions' . The more decay-resistant outer cuticle encloses altered organic material which shows no anatomical detail . In fine-grained lithologies, in particular, flattening obscures the original three­ dimensional morphology of the plant (e . g . the ar­ rangement of leaves on a stem), but this may be retained to some extent in coarser sediment (Rex & Chaloner 1983) . Experimental work by Rex and Chaloner (1983) showed that flattening of plant structures infilled by sediment (e .g. the woody cylin­ der of a Calamites stem) results in a 'compression border' formed by the plant tissue which compacts to a much greater extent than the sediment-fill which it surrounds . This border represents the original thickness of the plant tissue; lateral expansion is prevented by the confining sediment . Compaction may also result in external features of the plant being 'printed' onto the sediment-infill or cast (e .g. leaf-cushions onto a cortical-infill) . In exceptional circumstances plants are preserved in three-dimensional detail. This occurs when they are permineralized (because of precipitation of cal­ cium carbonate, silica, or pyrite), in which case they resist compaction (Section 3 . 10) . Soft tissue

Flattening of soft-bodied organisms is mainly the result of collapse due to decay . This exerts no pres­ sure on the confining sediment and therefore no lateral expansion occurs (although fluids may seep

245

beyond the outline of the specimen) . Collapse takes place within a very short time-scale (days or weeks), compared with compaction resulting from over­ burden pressure . Hence soft-bodied organisms are preserved in three-dimensions only where dia­ genetic alteration has taken place almost instantly. This kind of spectacular preservation most com­ monly involves phosphatization (Sections 3 . 8 .4, 3 . 1 1 .3) . In a number of Konservat-Lagerstatten (e . g . the Burgess Shale and Hunsriick Slate; Sections 3 . 1 1 . 2, 3 . 1 1 .4) turbulent transport and catastrophic burial (obrution; Section 3 . 6) have resulted in the pre­ servation of specimens in a variety of orientations to bedding. Studies of the Burgess Shale arthropods have shown that while the majority of the specimens come to rest with their most pronounced planar dimension near-parallel to the bedding (i. e . resul­ ting in lateral flattening in the case of bivalved arthropods, dorso-ventral in trilobites), a signifi­ cant proportion are oblique, lateral, or even vertical (Whittington 1985) . Restoration of flattened fossils

In organisms with mineralized skeletons the results of compaction are usually clearly evident as frag­ mentation, fracturing, or distortion of the shape. The original three-dimensional appearance can be established by comparison with the same or similar taxa preserved in more competent lithologies . Soft­ bodied and lightly skeletized organisms, however, are rarely preserved except in a flattened configur­ ation, and other methods have to be employed to restore them (Briggs & Williams 1981). As expansion of the outline does not occur, soft­ bodied fossils are only distorted by flattening nor­ mal to the plane of bedding. Thus a suite of fossils preserved in various orientations represents differ­ ent projections of the three-dimensional organism onto a two-dimensional bedding plane . In this re­ spect they are equivalent to a series of photographs of the original organism taken from different angles (Briggs & Williams 1981 ) . (This is the case even if the flattened fossil is not strictly two-dimensional many of the Burgess Shale fossils, for example, consist of discrete layers separated by a thin veneer of sediment . ) Based on this realization, models can be used to assist the restoration of flattened fossils. A simple three-dimensional model is made and then photographed in a variety of orientations (Fig. 2 ) . These photographs are directly analogous to flatten­ ing the organism onto a bedding plane . A systematic

3 Taphonomy

246

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Flattening of the telson of the Burgess Shale arthropod Odaraia alata . A, C, E, G, I, Model of telson photographed in different attitudes . B, D, F, H, J, Specimens of the telson preserved in different orientations to the bedding for comparison with the adjacent figure (B, D, x 1 . 2; F, H, x 1 .8; J, x O . 9) . The similarity of the specimens to the photographs of the model indicates that the restoration is essentially correct . (From Briggs & Williams 1981 . ) (Reproduced with permission from the Lethaia Foundation. ) Fig. 2

comparison of the photographs with specimens pre­ served in different orientations allows the resto­ ration to be tested, corrected, and refined (Briggs & Williams 1981) . This approach has been used, for example, with Burgess Shale fossils, and graptolites . The tilt correction control on a scanning electron microscope can be used also to restore small de­ formed fossils visually. The same approach can be applied using numeri­ cal methods . Doveton (1979) employed standard matrix algebra to compute three-dimensional resto­ rations of fossils based on morphological distances measured from specimens flattened in particular orientations to bedding. This involved a series of steps: (1) digitizing specific reference points on the fossils with reference to coordinates; (2) comput­ ing the estimated distances between these points; (3) computing a cross-product matrix and its eigen­ values and eigenvectors and generating a linear

coordinate solution; (4) modifying this solution, as appropriate, using non-linear mapping; and (5) dis­ playing perspective views of the non-linear solution to allow comparison and refinement with reference to other material . Fossils may be distorted tectonically, of course, in directions other than normal to bedding . They can be restored using computer-graphical methods . Such fossils (e . g . trilobites, brachiopods, crinoid ossicles) are useful in the analysis of strain in de­ formed rocks (Ramsay & Huber 1983) . If the fossil was initially spherical (e . g . Radiolaria), the shape of the strain ellipsoid can be determined directly . Deformed fossils are often flattened, however, in which case strain can be assessed in only one section through the strain ellipsoid (that parallel to bed­ ding) . While the principal axes can usually be ident­ ified, it may be possible to determine the magnitude of strain only semiquantitatively.

3 . 8 Diagenesis References Briggs, D . E . G . & Williams, S . H . 1981 . The restoration of flattened fossils. Lethaia 14, 157- 164. Doveton, J .H. 1979 . Numerical methods for the reconstruction of fossil material in three dimensions . Geological Magazine 116, 215-226.

Ramsay, J . G . & Huber, M.1. 1983. The techniques of modern structural geology. Volume 1 : Strain analysis . Academic Press, London.

247

Rex, G . M . & Chaloner, W . G . 1983. The experimental forma­ tion of plant compression fossils. Palaeontology 26, 231 252 .

Seilacher, A . , Andalib, F . , Dietl, G. & Gocht, G . 1976 . Pres­ ervation history of compressed Jurassic ammonites from southern Germany. Neues Jahrbuch for Geologie und Paliiontologie, Abhandlungen 152, 307-356. Whittington, H.B. 1985 . The Burgess Shale. Yale University Press, New Haven .

3 . 8 Diagenesis

3 . 8 . 1 Skeletal Carbonates M . E . TUCKER

Introduction

Many organisms have skeletons and shells com­ posed of calcium carbonate . The carbonate occurs in a great range of crystal sizes, fabrics, and mosaics, depending on the organism group . The skeletons of many organisms are composed of either aragonite or calcite, but some have both (Table 1 ) . After death, the carbonate skeleton is commonly altered to a greater or lesser extent during near-surface and burial diagenesis . In studies of fossils, an under­ standing of the diagenetic processes which have taken place is necessary to interpret the original mineralogy and structure of skeletons and shells. It also contributes to an interpretation of the organ­ isms in terms of taxonomic affinity, palaeoecology, and taphonomy. Thus there has been much dis­ cussion, for example, of the original mineralogy of extinct groups such as rugose corals, archaeo­ cyathids, and stromatoporoids . Aragonite is the mineralogy of many mollusc shells, all scleractinian coral skeletons, and many green calcareous algae, and it is mostly in the form of needle-shaped crystallites and tablets less than 20 J.lm in length . The aragonite in marine organisms is characterized by quite high strontium levels, from a few 1000 ppm in molluscs to 800 - 10 000 ppm in corals and green algae . Skeletal calcite is commonly

divided into two groups on the basis of magnesium content: low magnesium calcite with less than 4 mole percent MgC0 3 and high magnesium calcite with 1 1 - 19 mole percent MgC0 3 . The magnesium content depends not only on the organism but also on environmental factors, such as temperature and salinity . Red calcareous algae like Lithothamnion, for example, commonly show a decreasing magnesium content into higher latitudes. In addition to red algae, bryozoans and echinoderms have skeletal elements of high magnesium calcite . Some molluscs (oysters and scallops, for example), brachiopods, coccoliths, and many foraminifera have low mag­ nesium calcite shells and tests . The majority of the calcite crystals in these skeletal grains are on the scale of microns, but echinoderm calcite does consist of large, single crystals several millimetres across and coarse fibrous calcite crystals also on the milli­ metre scale occur in some skeletons (such as belem­ nites, certain foraminifera, and brachiopod spines) . The diagenesis of carbonate skeletons depends mainly on the original mineralogy, and also on the nature of the pore-fluids . Aragonite is a meta­ stable polymorph of CaC0 3 and is only preserved under special conditions, such as within imper­ meable, generally organic-rich mudrocks . In the majority of cases, within sandstones and limestones, aragonite is altered to calcite . Calcite, on the other hand, is the more stable form of CaC03 , and so is generally preserved. However, the magnesium content is usually reduced considerably, and there may be more diagenetic alteration of high mag­ nesium calcite grains than those originally of low magnesium calcite .

248

3 Taphonomy

The mineralogy of carbonate skeletons . x dominant mineralogy, (x) less common. During diagenesis these mineralogies may be altered or replaced; aragonite, in particular, is metastable and is almost always replaced by calcite, and high magnesium calcite loses its magnesium. (From Tucker 1981 . )

Table 1

=

=

Mineralogy

Organism Mollusca: Bivalves Gastropods Pteropods Cephalopods Brachiopods Corals: Scleractinian Rugose + tabulate Sponges Bryozoans Echinoderms Ostracodes Foraminifera: Benthic Pelagic Algae : Coccolithophoridae Rhodophyta Chlorophyta Charophyta

Aragonite

x x x x

Low Mg calcite

High Mg calcite

x

x

Aragonite + calcite

(x) x

(x ) (x)

x x x

(x )

x x

x

x x x x x

x

x x x

x x

Diagenesis of skeletal aragonite

Skeletal aragonite is commonly altered to calcite and this takes place in two main ways : by wholesale dissolution and later filling of the void by calcite cement, and by a neomorphic replacement process of dissolution- reprecipitation across a thin film, referred to as calcitization (Bathurst 1975) .

Wholesale dissolution of aragonite mostly occurs where pore-fluids are well undersaturated with respect to CaC0 3 ; this is generally the case in near­ surface meteoric diagenetic environments, particu­ larly in the vadose zone (above the water table) where there is a high throughput of water. Dissol­ ution of the aragonite leaves a void, with the orig­ inal shape maintained either by an earlier, calcitic cement fringe around the shell or by a micritic envelope, a thin zone of alteration around the shell produced by endolithic algae (Fig. 1). When pore­ fluids become supersaturated with respect to CaC0 3 , calcite is precipitated within the skeletal voids . This calcite is actually a cement, and so commonly shows a drusy fabric of increasing crystal

x x

size towards the void centre . The timing of the calcite precipitation is variable . It may be early, soon after the dissolution, possibly in the lower vadose zone or phreatic zone (below the water table) if the meteoric waters have quickly become saturated in CaC0 3 . Alternatively, the skeletal voids may not be filled until later in diagenesis, during burial. This may be evident from the fracture of micritic envelopes and cement fringes into the voids, indicating some degree of compaction by overbur­ den pressure before calcite precipitation.

Calcitization of aragonite skeletons and shells pro­ duces textures which generally retain relics of the original structure . The most common relic is that of growth banding (Fig. lA), preserved in the form of organic particles in the replacement calcite crys­ tals. Relic fragments of the original aragonite itself may be preserved in the calcite, and these are best seen with the scanning electron microscope after very delicate etching (e .g. 0 . 5% formic acid for 30 s) of a polished thin section (Sandberg & Hudson 1983) . The aragonite relics may have been protected from dissolution by an organic sheath . The calcite

3 . 8 Diagenesis

249

within the original shell; they may develop along the growth banding for example, but cross-cutting relationships are common (Fig . lA) . The replacement calcite is commonly a pale amber to brown colour, and in thin section a pseudopleo­ chroism (a variation in colour intensity when the stage is rotated) is usually seen, attributed to the effects of minute particles of organic matter. The timing of calcitization is also variable . It may occur in near-surface or in burial diagenetic environments, and if in the latter, a post-compaction origin can be deduced from the nature of fracture surfaces (follow­ ing original shell structure) if there was sufficient overburden to break the grains . Since in calcitization the replacement of skeletal aragonite takes place across a thin film, probably a few microns thick, with dissolution of aragonite on one side and precipitation of calcite on the other, most of the CaC03 is derived from the shell. The replacement calcite is thus commonly enriched in strontium (over calcite cement), inherited from the aragonite . Changes in pore-fluid chemistry or fluid flow during the replacement process may lead to an increase in width of the replacement front, to such an extent that dissolution of the aragonite may proceed faster than precipitation of the calcite, and a significant void may be developed . This may be filled later by calcite cement. Thus some originally aragonitic skeletons may show both types of pres­ ervation : calcite cement in dissolution voids and neomorphic spar through calcitization . Diagenesis of skeletal calcite

Fig. 1 A, Formerly aragonitic bivalve shell replaced by calcite . Large neomorphic calcite crystals contain relics of the original shell structure. The bivalve was bored prior to replacement and is surrounded by a micrite envelope . Diagenesis took place in the meteoric vadose zone, as indicated by the meniscus calcite cement between the two bioclasts . B, Two bivalve shells originally of aragonite which underwent dissolution; calcite spar was then precipitated within the shell voids. Both shells have micrite envelopes which maintained the shell shape . Calcite spar is also the cement between the bioclasts and was precipitated from meteoric water. Both from the Pleistocene, Miami, Florida . Photographed in plane-polarized light .

crystals replacing the aragonite are generally coarse, certainly much larger than the original aragonite crystals, and they do not show any drusy fabric. The crystals may in part follow lines and planes

In general, ancient carbonate skeletons and shells originally composed of calcite are still composed of calcite (unless silicified or dolomitized) and show good to perfect preservation of the original skeletal structure . Biogenic grains originally composed of high magnesium calcite, however, may show some alteration, and even low magnesium calcite shells, such as brachiopods, under the close scrutiny of cathodoluminescence, may be seen to have patches of recrystallized calcite with different iron and manganese contents . With high magnesium calcite 2 skeletal elements, the Mg + content is reduced to a few mole percent MgC0 3, but commonly small crystals (5 - 20 [tm) of dolomite are produced within the skeleton through stabilization to low magnesium calcite . These microdolomites can be seen in thin section, but they are best viewed under cathodo­ luminescence or with the scanning electron micro­ scope as slightly etched polished surfaces .

250

3 Taphonomy

Microdolomite is a common constituent of ancient echinoderm fragments, confirming an original high magnesium calcite mineralogy . The identification of an original high magnesium calcite skeleton is still possible, even where microdolomites are absent: the calcite may retain a 'memory' in the form of several mole percent MgC03, and this is generally significantly higher than originally low magnesium calcite grains, which usually contain less than 1 mole percent MgC0 3 after diagenesis . Originally high magnesium calcite grains may also pref­ 2 erentially take up iron (Fe + ) during diagenesis (identified by staining), if this is available in the pore-fluids . Rarely, re crystallization fabrics (patches of coarse calcite crystals) may develop in high mag­ nesium calcite grains, and even small cavities and voids may form as a result of localized dissolution. Calcitic skeletons and shells are commonly the sites of syntaxial (in optical continuity) cement pre­ cipitation. The most familiar are overgrowths on echinoderm grains, whereby large cement crystals are formed . Fibrous calcite cements are commonly precipitated syntaxially on brachiopod, trilobite, and pelagic bivalve shells, and much hard chalk and chalkstone is the result of calcite overgrowth on coccolith debris . Many limestones, and the fossils they contain, have been subjected to dolomitization. The preser­ vation of carbonate skeletons again depends not only on their original mineralogy, but also on the timing of the stabilization of aragonite and high magnesium calcite to low magnesium calcite . If dolomitization occurs before CaC0 3 mineral stabili­ zation, carbonate skeletons of high magnesium calcite commonly display perfect fabric retention . Echinoderms, benthic foraminifera, and red cal­ careous algae fall into this category. Aragonite shells, on the other hand, are usually dissolved out and the voids filled with dolomite cement. Low magnesium calcite is much more resistant to dolo­ mitization and commonly survives, or is replaced with fabric destruction . If dolomitization takes place after a carbonate sediment has been stabilized to calcite, then mostly the skeletons show very poor structural preservation. There is a broad pattern of change in the miner­ alogy of carbonate skeletons through the Phan­ erozoic . Calcite dominates in the Palaeozoic, aragonite becoming increasingly important in shallow-water carbonate skeletons and shells from the Mesozoic into the Cenozoic. Such changes may reflect subtle changes in seawater chemistry (Tucker 1989) .

References R . G . C . 1975 . Carbonate sediments and their diagenesis. Elsevier, Amsterdam. Sandberg, P.A. & Hudson, J . D . 1983 . Aragonite relics in Jurassic calcite-replaced bivalves . Sedimentology 30, 879 -

Bathurst,

892 . Tucker, M . E . 1981 . Sedimentary petrology. Blackwell Scientific Publications, Oxford. Tucker, M . E . 1989 . The geological record of carbonate rocks. In: M.E. Tucker & V.P. Wright (eds) Carbonate sedimentology. Blackwell Scientific Publications, Oxford .

3 . 8 . 2 Carbonate Nodules and Plattenkalks P . A . ALLISON

Preservation of soft parts i s more commonly associ­ ated with carbonate mineralization than with any other authigenic mineral. Such preservation occurs in localized concentrations of authigenic carbonate referred to as concretions or nodules, and also in fine-grained bedded limestones known as

plattenkalks . Nodules

Fossil-bearing carbonate (siderite or calcite) nodules are usually associated with organic-rich argillaceous sediments . The fossils within such nodules are often preserved in three dimensions and occasionally include preserved soft parts . Fossil-bearing carbon­ ate concretions are commonly 10 - 30 cm in size, although examples up to 10 m long enclosing com­ plete plesiosaurs have been recorded . The shape of concretions is controlled by sediment porosity. In sandstones, where porosity in both vertical and horizontal planes is equal, nodules are spherical. In argillaceous sediments, on the other hand, porosity is greater in the horizontal plane and the nodules that form are greater in dimension parallel to bedding. If sediment permeability in the horizontal plane is uniform then the nodules tend to be discoidal; if not, an ellipsoidal form occurs with the long axis aligned in the direction of greatest permeability . Concretionary carbonate is rarely replacive and is usually precipitated in sediment pore-spaces . The presence of undeformed delicate biogenic structures

3 . 8 Diagenesis such as burrows and faecal pellets shows that min­ eral precipitation did not force sediment particles apart. Thus, the volume of nodule-forming mineral is equal to sediment porosity at the time of carbonate precipitation (Raiswell 1976) . Sediment compaction in mud rocks is proportional to depth of burial; hence an assessment of original porosity in carbon­ ate concretions is also an indication of diagenetic timing. In the case of carbonate concretions, this original porosity will be approximately equivalent to the acid soluble fraction of the nodule . Using this method, internal porosities of certain concretions can be shown to be as high as 80- 90% at the centre (Raiswell 1976) . Since such porosities in mudrocks only occur in the upper 10 m of the sediment, an extremely early diagenetic origin can be inferred . Internal porosities a t the rim o f the concretion, however, may be as low as 50% . Thus it is clear that nodule growth is often initiated early in the burial history of a sediment and continues during sedi­ ment compaction . Fluctuations in minor and trace element chemistry and in stable isotopes between the centre and the rim of a concretion therefore indicate variations in pore-water chemistry during burial. Early diagenetic mineralization, such as that responsible for nodule formation, is the only process capable of retarding information loss during decay and fossilization . For this reason fossils preserved in nodules generally exhibit a higher level of pre­ servation than those in the host sediment (Section 3 . 1 ) . For example, the Upper Carboniferous Mazon Creek biota of Illinois, U.5.A. (Section 3 . 1 1 . 5) includes a variety of plants and animals with soft parts, but these only occur in siderite nodules and are unknown from the host shale . Similarly, ammon­ ites preserved within concretions in the Upper Lias of Yorkshire are typically uncompacted, whereas those in the host sediment are often flattened with compaction cracks (see also Section 3 . 7) . Concretions characteristically display a network of radial and concentric fractures known as septaria (Fig. 1 ) . It was once thought that these accom­ modated the reduction in volume brought about by dewatering of clay minerals during diagenesis . However, Astin (1987) has shown that such fracture systems are merely a response to overburden pres­ sure during burial and can form at depths of less than 50 m.

Process offormation. The input of organic detritus to a sedimentary sequence and its subsequent decay (see also Section 3 . 1) are the primary factors control-

251

Fig. 1 Septarian cracks in calcareous concretion from Jurassic of Lyme Regis, Dorset. Specimen is 20 cm in diameter.

ling degree of anoxicity, Eh, pH and thereby min­ eral paragenesis . In the presence of oxygen, organic carbon in sediment is broken down by aerobic microbial respiration and CO2 is produced. In pore­ water solution this produces carbonic acid which promotes carbonate dissolution. In the absence of oxygen the sediment microbiota utilize a series of alternative oxidants in the respiration process, such as manganese, nitrate, iron, or sulphate . These reactions have different free-energy yields and this governs their occurrence in sediment. In the ideal case they are layered (Fig. 2) with those liberating the greatest amount of free energy at the top of the sediment pile . The depletion of the oxidants initiates the next most efficient reaction. When all the oxidants have been depleted fermentation reactions dominate and methane is produced. A common denominator in all of these anaerobic reactions is the production of the bicarbonate ion. If this reacts with any suitable cations, such as calcium, iron, magnesium or manganese, then a carbonate mineral may form. The formation of early-diagenetic carbonate concretions is therefore associated with anaerobic decay of organic carbon . The mineral formed is dependent upon the dominant decay pathway at the site of deposition . In a marine system calcium is normally present in supersaturation levels; calcite is the most stable mineral phase and

3 Taphonomy

252 A E RO B I C N i t rate red u ct i o n u

Manganese red u c t i o n

et: lJ.J

I ro n red u c t i o n

co

o

«

Z

«

CHP + 7C02

+

4Fe(OH)3

---7

4Fe + +

+

8HCO) + 3Hp

S u l p h ate red u c t i o n Fig. 2 Idealized bacterial reduction zones in organic-rich sediment. (After Berner 1981 . )

Methanoge n e s i s

iron reacts preferentially with sulphide ions (from sulphate reduction) to produce pyrite (Section 3.8.3). In a freshwater system, however, sulphide ions are almost absent and concentrations of iron ions may exceed those of calcium to a degree which allows siderite to form (Berner 1981) . Although there are exceptions (Sellwood 1971), siderite can be con­ sidered an indicator of freshwater conditions . The manganese content of pore-water is rarely high enough for manganous mineral species to form . Manganese ions liberated near the anoxic- oxic boundary by anaerobic respiration are therefore more commonly incorporated into other mineral species such as calcite or siderite . Since manganese reduction is one of the earliest reduction zones in the sediment pile, concentrations of manganese in pore-water solution are greatest near the anoxic ­ oxic interface . Thus, those phases of the concretion which form first (the centre) have a higher manganese - calcium ratio than those which form later (the rim of the concretion) . Berner (1968) suggested a model for the localized precipitation of carbonate (forming concretions) based upon a series of actualistic experiments using decomposing fish. He monitored the decay of fish in jars containing anoxic seawater and noted the effect on pore-water chemistry. As fish decayed, ammonia and bicarbonate were liberated to solution and produced an alkaline environment; at the same time calcium stearate (a soap) formed at the bot­ tom of the jars containing the fish . Berner (1968) suggested that this stearate was the most stable calcium-bearing mineral phase around a decom­ posing carcase . He believed that the authigenic carbonates were formed from the additional bicar­ bonate generated by further decomposition after the depletion of available stearate . Precipitation in this case would be favoured by the high pH micro­ environment around the decomposing carcase .

Raiswell (1976), however, based an alternative model upon a geochemical and petrological study of ammonite-bearing concretions from Lower Jurassic shales in North Yorkshire, England . Stable isotope analysis of these concretions showed that the car­ bonate fraction had been generated as bicarbonate ions during bacterial sulphate-reduction and methanogenesis . However, the decay of the en­ closed organisms (e .g. ammonites, belemites) could not have liberated sufficient bicarbonate to produce the volume of calcite forming the concretions . The bicarbonate was generated b y the decay of disseminated organic carbon, and it migrated to nucleation sites such as skeletal carbonate . Localized precipitation of authigenic carbonate around such sites produced concretions . In an open geological system, where calcium levels can be replenished, carbonate species can form in the decay aureole of decomposing organisms . Carbonates precipitated in this fashion may func­ tion as nucleation centres for additional bicarbonate in pore-water solution . Problems arise, however, in modelling the growth of carbonate concretions around plants in fossil peat swamps (see also Section 3 . 10) . When plants decompose they liberate humic and fulvic acids and produce low pH pore­ waters which inhibit carbonate formation . It is possible that bicarbonate ions produced during anaerobic decay achieve a sufficiently high concen­ tration to buffer acid pore-waters and promote car­ bonate formation . Alternatively, nodules may form in peat swamps which have been flushed by non­ acidic pore-waters . Evidence to date is inconclusive . Plattenkalks

Plattenkalk deposits (also referred to as lithographic limestones) occur in both lacustrine and marine set­ tings and are characteristically fine-grained and well

253

3 . 8 Diagenesis bedded . Examples include the Eocene Green River Formation of central North America, the Cretaceous Haqel and Hjoula Limestones of Lebanon, and the celebrated Solnhofen Limestones of the Jurassic of Bavaria (Section 3 . 1 1 .7) . The carbonate in these deposits may originate from a biogenic source (such as calcareous algae) or as a chemical precipi­ tate . The formation of such deposits is therefore favoured by a reduced supply of terrigenous sedi­ ment and a high rate of organic production. Plattenkalk deposits are famous sources of well preserved fossils, which in some cases include soft parts . Exceptional preservation in this case is favoured by rapid burial and a general absence of benthos . Soft-bodied fossils from such deposits are usually flattened parallel to bedding; thus lithifi­ cation occurred after decay-induced collapse of soft­ tissues (such as skin and muscle) and compaction of lightly skeletized structures (such as arthropod cuticle) . References Astin, T . R. 1987. Septarian crack formation in carbonate concretions from shales and mudstones. Clay Minerals 21, 617-631 .

Berner, R.A. 1968. Calcium carbonate concretions formed by the decomposition of organic matter . Science 159, 195 197.

Berner, R.A. 1981 . Authigenic mineral formation resulting from decomposition in modern sediments. Fortschrifte der Mineralogie 59, 1 1 7- 135. Raiswell, R. 1976 . The microbial formation of carbonate con­ cretions in the Upper Lias of N . E . England . Chemical Geology 18, 227- 244. Sellwood, B.W. 1971 . The genesis of some sideritic beds in the Yorkshire Lias (England) . Journal of Sedimentary Petrology 38, 854-858.

pyrite is best understood . Studies of recent sedi­ ments have shown that the formation of authi­ genic pyrite can occur very early in the diagenetic history of a sediment and may be initiated only a few centimetres below the sediment- water interface (Berner 1984) . In the presence of oxygen, microbes feed on organic carbon in sediment and respire aerobically (Section 3 . 1 ) . With in­ creasing organic content and/or depth of burial the diffusion of oxygen into the sediment is impeded and the microbes are forced to respire anaerobically. In a marine environment the princi­ pal anaerobic decay pathway is that of sulphate­ reduction (Bern er 1972, 1984) . This process can be represented by the following equation: 2CH20 + sol-

=t

H2S + 2HC0 3 - .

However, according to Jorgenson (1982) this reac­ tion actually progresses through a variety of stages, including the breakdown of organic biopolymers (by bacterial fermentation) to simpler organic mol­ ecules that can fuel sulphate-reducing reactions . A principal by-product of this reaction is hydrogen sulphide (H2S) which can combine with reactive iron-bearing minerals to produce finely-particulate iron mono sulphides (FeS) such as greigite and mackinawite (Fig. 1 ) . Bacterial breakdown of H2S liberates sulphur (S) to solution which can react with FeS to produce pyrite . Should these sulphur­ bearing chemicals diffuse upwards into aerobic waters they can be broken down by oxidizing bacteria to liberate sulphates to pore-water solution (Fig . 1 ) . Fossil preservation

Process of formation

Mineralization is the most frequent means of halting the information loss associated with the decay of macro-organisms (Section 3 . 1 ) . Organisms that are permineralized early in the diagenetic history of a sediment frequently exhibit higher levels of preservation than those that form later (Allison 1988) . Early diagenetic minerals (such as pyrite) are therefore an important preservational medium for fossils . The preservation of fossils is a result of the interplay between decay and mineralization. This can be simply illustrated with respect to pyrite .

Sedimentary pyrite is frequently encountered as a minor component of both modern (Berner 1972) and ancient (Baird & Brett 1986; Allison 1988) fine-grained marine clastic sediments . Of all the early diagenetic mineral phases, the formation of

Soft tissues. With rapid mineralization and/or an impediment to the decay processes, soft tissues such as muscle may be pyritized . Examples of this type of preservation include the appendages of trilobites from the Ordovician: Beecher's 'Triarthrus'

3 . 8 . 3 Pyrite P . A . ALLISON

3 Taphonomy

254

by sulphate-reducing bacteria and is replaced by pyrite; even polished thin-sections show little or no cellular detail. The late wood, however, being more resistant to the action of sulphate-reducing bacteria, forms a coalified residue which preserves cell walls infilled with pyrite (Fig. 2C) .

Shell and bone. Biogenic hard parts such as shell (calcium carbonate) and bone (calcium phosphate) are some of the most decay-resistant biological structures, and as such are the most commonly occurring fossil types. Of the two, calcium carbonate is the more unstable and is therefore the more likely to be replaced by pyrite . Preservation of shells may include replication of original shell lamination (Fig. 2D) . Mineral form Pyrite

Sedimentary pyrite occurs in a variety of mor­ phologies (Allison 1988) .

Fig. 1 Summary of the geochemical processes involved in the formation of pyrite . (From Berner 1972 . )

Trilobite Bed of New York State, U . S . A . , and the preservation of trilobites and the soft-tissues of cephalopods from the Devonian Hunsruckschiefer of the Bundenbach district of West Germany (Section 3 . 1 1 .4) . Refractories. With more decay and delayed pyrite formation, soft tissues will be destroyed and only decay-resistant biological compounds (termed refractories) such as cellulose and lignin are pre­ served. Of the two compounds, lignin (a complex aromatic molecule) is the most refractory; thus lignified plant remains have a higher preservation potential than purely cellulosic tissues. This decay­ rate differential can result in a preservational bias between different anatomical elements of a plant. For example, growth rings are composed of two elements : early wood, laid down at the beginning of the growing season (spring); and late wood, laid down later in the season (summer) . Early wood is characterized by large thin-walled cells with a low lignin content, while late wood is usually composed of smaller thick-walled cells with a higher lignin content . Early wood is therefore more amenable to decay than late wood and in a sulphate-reducing environment is more likely to be pyritized . Pyritized wood from the Eocene London Clay of Kent, England displays just such a bias (Allison 1988) . The early wood has been completely degraded

Fig. 2 Examples of pyrite morphotypes from the Eocene London Clay of Kent, England. A, Pyrite stalactites hanging from the inside of a gastropod shell . B, Thin-section of bone (light-grey) with pyrite-infilling of cavities . C, Preservation of grain in wood. Light-coloured layers are pyritized early­ wood, dark layers are coalified late-wood . D, Pyritized gastropod shell, outer margin of shell towards top of picture. Note preservation of original shell lamination (left-to-right) in pyrite. (From Allison 1988 . )

3 . 8 Diagenesis

Framboids. Spherical aggregates of microcrystalline cubes and octagons are commonly encountered in mud-grade sediments . They vary in size from a few microns to about 1 mm in diameter and are referred to as framboids (from the French framboise meaning raspberry) . They may occur as isolated elements or as conjoined aggregates, the latter occurring as linear (picking out original bedding) or sub-spherical amalgamations .

Pyritized sediment. Sediment infills of biogenic cavities which have been cemented by pyrite are referred to as pyritized sediment. Pyrite may replace detrital grains . Cavity linings . Euhedral pyrite linings of cavities are common in mud-grade sediments . Examples of such cavities include the living space of molluscs and brachiopods, and vesicles in bone (Fig . 2B) . They may b e completely infilled o r only partially lined with pyrite . In some cases pyrite stalactites (Fig. 2A) hang down from these linings and form geopetal structures .

Pseudomorphic textures . Pyrite may replace detrital and authigenic minerals as well as fossils . In the Eocene London Clay of Kent (Allison 1988) pyrite pseudomorphs authigenic cavity-lining calcite and phosphate concretions . In the latter, pyrite com­ monly extends from pyrite-infilled septaria and replaces the authigenic phosphate and detrital minerals of the concretion. Such pyritization in­ cludes the preservation of sedimentary textures such as original bedding, burrows, and faecal pellets .

Overpyrite. Encrusting pyrite on the surface of fossils is termed overpyrite. Concretions. Pyrite concretions adopt a variety of habits and crystal textures . It is generally assumed that tabular examples formed later in the diagenetic history of a sequence when porosity was greater in the horizontal plane than in the vertical plane . Cone-in-cone pyrite is common and is thought to have formed as a result of the interference between overburden pressure and pressure of crystallization during mineral formation.

Reworked pyrite. As an early diagenetic mineral that can form in the upper few centimetres of sedi­ ment, pyrite is extremely susceptible to reworking. However, it was long assumed that reworked pyrite would be oxidized and destroyed during the pro-

255

cess. Recent work in the Devonian Leicester Member flooring the black shales of the Genesee Formation of New York State (Baird & Brett 1986), however, has demonstrated the presence of reworked pyrite remanie horizons . It is thought that these deposits were concentrated during brief erosive phases in an otherwise anaerobic environment. Palaeosalinity

The formation of pyrite is controlled by the concen­ tration of organic carbon, dissolved sulphate, and detrital iron minerals (Berner & Raiswell 1984) . In a normal marine environment iron minerals and sulphates are present in abundance, and pyrite formation is controlled by the supply of organic carbon. In freshwater environments, however, the formation of pyrite is limited by low sulphate con­ centration. Euxinic environments, on the other hand, are characterized by an abundance of H2S (from anaerobic sulphate reduction); the limiting factor for pyrite formation in this type of environment is therefore the availability of detrital iron minerals . The factors controlling pyrite formation in these different environments produce characteristic ratios of carbon and pyrite sulphur in a sediment, which can be used in the determination of palaeosalinity (Berner & Raiswell 1984) . References Allison, P.A. 1988. Taphonomy of the Eocene London Clay biota . Palaeontology 31, 1079 - 1100 . Baird, G . c . & Brett, C . E . 1986 . Erosion o n a n anaerobic sea­ floor: significance of reworked pyrite deposits from the Devonian of New York State . Palaeogeography, Palaeo­ climatology, Palaeoecology 57, 157- 193. Berner, R.A. 1972. Sulfate reduction, pyrite formation and the oceanic sulfur budget. In : D. Dyrssen and D. Jagner (eds) The changing chemistry of the oceans, Nobel Symposium No . 20, pp . 347 - 361 . Almquist and Wiksell, Stockholm. Berner, R.A. 1984. Sedimentary pyrite formation: an update . Geochimica et Cosmochimica Acta 48, 605 - 615. Berner, R.A. & Raiswell, R. 1983 . A new method for dis­ tinguishing freshwater from marine sedimentary rocks. Geology 12, 365 - 368. Jorgensen, B . B . 1982 . Ecology of the bacteria of the sulphur cycle with special reference to anoxic - oxic interface environments . Philosophical Transactions of the Royal Society of London B298, 543 - 561 .

256

3 Taphonomy

3 . 8 . 4 Phosphate L . P RE V O T & J . L U C A S

Phosphorus is an element critical to life . It i s con­ centrated either in hard tissues, such as bones or some cuticles, or more often in soft parts (which have an almost constant composition: Cso, NIS PI) . ' Therefore it is not surprising that it is involved in fossilization . Bones, teeth, and scales, being prima­ rily phosphatic, have a high preservation potential . Skeletons in other material (e .g. calcite, silica), and soft tissue, may be diagenetically altered to phosphate if there is enough organic matter available . Fossil preservation

Primary phosphate. The vertebrate skeleton is com­ posed mainly of hydroxyapatite (CalO(P04)6(OH)z) . Locally, especially in teeth, some of the OH- ions may be replaced by F- ions, resulting in a less soluble hydroxy-fluorapatite . Phosphatic invert­ ebrate shells have variable but similar compositions . The composition of fossil bone generally differs in having substantially more fluorine . For example, the average fluorine content of the bones of marine and freshwater fish is 4300 ppm and 300 ppm re­ spectively, whereas those of their fossil counter­ parts contain 22 100 ppm and 19 900 ppm fluorine . Some pol - is replaced by co l - (one pol - re­ placed by C0 32 - + F-, or 2P043 - replaced by 2 2co l - + 1 vacancy of Ca + ) and all the OH- by F- . The primary hydroxyapatite is transformed into less soluble carbonate-fluorapatite by simple ion exchanges between solution and mineral, without the necessity of a dissolution stage . This alteration occurs without any modification of the shape and structure of the object.

ation of calcareous organisms into apatite has been demonstrated in the laboratory (Lucas & Prevot 1985) . These observations and experiments suggest the following possible mechanism: (1) the phos­ phorus needed to replace carbonate by apatite is added to the sediment by organic matter; (2) various micro-organisms (e .g. bacteria, algae, fungi) promote decay, liberating po l - ions and making the interstitial water acidic . This acidification, which may be very localized, results in the dissolution of carbonate; and (3) the newly liberated P043 combines with Ca2 + to form apatite . Apatite forms preferentially at the carbonate - micro-organism interface and replaces the dissolved carbonate . Crystallization of apatite preserves the external shape of the originally calcareous shell . Here, as in the fossilization of primary apatite, fluorine also plays an important role, for the final composition is carbonate-fluorapatite . Phosphatization of primary silica also occurs in radiolarian tests, e . g . in phosphate deposits . This process is poorly understood .

Un mineralized organic material. Microscopic examin­ ation of phosphorites shows that numerous micro-

Calcium carbonate. Shells and tests composed of calcium carbonate, either calcite or aragonite, may be preserved in sediment if the physico-chemical properties of the interstitial waters remain similar to average marine or freshwater conditions (Section 3 . 8 . 1 ) . Such carbonate debris may also be altered to apatite without affecting external morphology (Fig. 1). In natural environments, this diagenetic alter­ ation occurs mainly in association with phosphate deposits (Prevot & Lucas 1986) . Bacterial transform-

Fig. 1 Foraminiferan, originally calcium carbonate, transformed into apatite in a phosphorite from Ganntour Basin (Morocco) . Thin section photomicrographs. A, Plane­ polarized light. B, Crossed polar light. The walls are in anisotropic apatite and the chambers filled with isotropic apatite .

3 . 8 Diagenesis organisms without shells (e.g. algae, fungi, bacteria) are fossilized in apatite, although they did not con­ tain any mineral precursor . Phosphatized coprolites (see also Section 4. 12) are well known . The organic matter itself is replaced by apatite which retains the exact shape of the object as shown, e . g . by the constriction striae on some coprolites . Even phos­ phatized soft tissues of arthropods (copepods, ostracodes) may occur in calcareous nodules and phosphatic nodular limestones, or in big vertebrate coprolites . The cuticle is replaced and/or coated by carbonate-fluorapatite (Muller 1985; Section 3 . 1 1 .3) . In this case the mechanism i s less clear, but may be similar to that in laboratory experiments where apatite is precipitated from solution by introducing phosphorus as a soluble organic complex, and calcium as a soluble mineral salt. The mechanism must be extremely rapid to account for the preser­ vation of faeces and of the finest details of micro­ scopic arthropods (Section 3 . 1 1 .3) without deformation . Conditions for phosphatization

Both the study of phosphorites and the results of experimental apatite synthesis allow an estimate of the most likely conditions for apatitic fossilization . Because of its stability requirements, apatite forms preferentially in an oxygen-depleted environment, sometimes even in fully reducing conditions, as indicated by the frequent association of pyrite with phosphates . This environment is easily produced by abundant organic matter, which is also required as the main source of phosphorus. The concentration of fluorine, essential to the formation of the more stable fluorapatite, is generally higher in marine than in freshwater. Its concentration in sedimentary apatites is so high that a constant supply is indi­ cated, suggesting a marine origin . However, sea­ water contains a high concentration of magnesium, well known to inhibit apatite formation. This cannot be eliminated under normal marine conditions, but may be removed in the pore-water of a mud during early diagenesis . These conditions of early diagenesis with an organic-rich marine mud also

257

control the formation of sedimentary phosphorite deposits, archetype of the environment for phos­ phogenesis . In the deposits of the Cretaceous ­ Tertiary transition, for example, phosphate-rich levels often contain abundant bones and teeth of marine vertebrates . Rare invertebrate skeletons are phosphatized . In contrast, the interbedded carbonates are rich in shells but almost devoid of phosphatic remains . This separate distribution of phosphatic and calcareous remains is due only to different conditions of fossilization: calcareous skeletons are well preserved in carbonate-rich levels, apatitic remains in phosphate-rich levels . For the same reason bones and teeth are only found in the phosphorite 'patches' (including nodules and coprolites) within the Cretaceous chalk of the Paris Basin, and not in the chalk itself. Though carbonate-fluorapatite appears most frequently in natural environments during early diagenesis, it is not the most stable of the apatites . Therefore it tends to evolve slowly into the more stable fluorapatite . The primary apatite loses its CO 2 very slowly; to reach the final stage takes several hundred million years . Phosphatic fossils occur mostly in phosphate deposits, and there the mechanisms of apatite genesis can be investigated . Knowledge of the palaeogeographical, palaeoclimatic, and other con­ ditions which result in apatite formation in phos­ phate basins is now increasing . It is still puzzling how these conditions converge locally to form phosphatic nodules in chalk, or to protect an isolated bone fragment . Apatite formation is far from fully understood . References Lucas, J. & Prevot, L. 1985 . The synthesis of apatite by bacterial activity: mechanism . Sciences Geologiques, Memoires 77, 83 - 92. Miiller, K.J. 1985 . Exceptional preservation in calcareous nodules. Philosophical Transactions of the Royal Society of London B311, 67- 73 . Prevot, L . & Lucas, J. 1986 . Microstructure o f apatite replacing carbonate in synthesized and natural samples . Journal of Sedimentary Petrology 56, 153 - 159.

3 . 9 Taphofacies C . E . B RETT & S . E . SPEYER

brachiopods); (6) degree and type of abrasion, cor­ rosion, or bioerosion of skeletons; (7) type of shell fillings or coatings; (8) evidence for early dissolution of skeletons; and (9) any special features of preser­ vation. By defining indices based upon taphonomic properties (e .g. ratio of articulated versus disarticu­ lated skeletons), it is possible to quantify various modes of fossil occurrence and to provide a basis for comparing the preservational grade of fossil assemblages. The differential preservation of similar fossils between facies reflects different biostrati­ nomic and/or diagenetic processes active in various environments . The most useful fossils for compara­ tive taphonomic study are eurytopic taxa that occurred in a variety of sedimentary environments . Comparative study of taphofacies permits recog­ nition of certain environmental parameters which influence preservation. These factors include par­ ticularly: (1) the relative frequency of episodic storms and other disturbances; (2) the relative rates of background sedimentation; (3) the environmen­ tal energy, including intensity and direction of currents; and (4) the geochemistry and level of

Taphofacies, or taphonomic facies, consist o f suites of sedimentary rock characterized by particular combinations of preservational features of the contained fossils (Brett & Baird 1986) . As such they are similar to, but distinct from, biofacies (Section 4. 18) which are defined on the basis of recurring organisms, generally species or genera, which are inferred to have lived together in the geological past. Similarly, taphocoenoses, or death assem­ blages, are simply groupings of organisms found together in fossil assemblages, whereas thanato­ coenoses are interpreted as variously biased deri­ vatives of once-living communities, or biocoenoses (see also Section 3 . 5) . In contrast, taphofacies are not defined on the basis of fossil taxa, but rather on the basis of consistent preservational properties . These preservational features include the following: (1) orientation of fossils, including life orientations; (2) relative degree of articulation of skeletons; (3) relative fragmentation of fossils; (4) proportion of convex-up to convex-down skeletons; (5) proportions of various skeletal elements from multiple-element skeletons (e . g . pedicle -brachial valve ratios in

Relationship of biostratinomic features of various types of fossil skeletons to sedimentation rate and environmental energy. (From Brett & Baird 1986 . )

Table 1

Sedimentation rates Environmental energy High

Skeletal type

Episodic, very rapid 2 (10 - 50 cm!10 years)

Low- intermediate (1 - 10 cm/103 years)

Fragile; ramose

Minor fragmentation

Strong fragmentation

Absent

Bivalved shells

Mostly articulated; rarely

Partially articulated; some fragmented

Disarticulated; fragmented; abraded

Partially articulated; pieces sorted

Disarticulated; pieces sorted

in situ

Low

Intermediate -rapid (1O - 100/cmJl03 years)

Multielement skeletons

Mostly articulated; rarely

Fragile; ramose

Intact; not fragmented

Some fragmentation

Strong fragmentation; corrosion

Bivalved shells

Articulated; some in situ

Mostly disarticulated; complete valves

Disarticulated; minor fragmentation; corrosion

Multielement skeletons

Completely articulated; some in situ; intact moults

Partially articulated; non-sorted

Disarticulated; non-sorted

in situ

258

259

3 . 9 Taphojacies Relationships of early diagenetic features of fossils (e .g. types of shell fillings, coatings, authigenic minerals) to sedimentation rate and oxygenation of bottom water and sediment. (From Brett & Baird 1986 . )

Table 2

Sedimentation rates

Water oxygenation

Sediment geochemistry

Episodic, very rapid 2 ( 1 - 50 cm/l0 years)

Intermediate - rapid (10- 100 cm/l03 years)

Low-intermediate (1 - 10 cm/l03 years)

Aerobic O2 > 0 . 7 mIll

Oxic- depth; organic-poor

No sediment fillings; late diagenetic mineral fillings; minor pyrite

Sediment steinkerns

Partial sediment steinkerns; rare chamositic, hematitic coatings

Aerobic- dysaerobic O2 0 . 7 - 0 . 3 mill

Anoxic with oxic microzone; organic-poor (non-sulphidic)

Pyrite steinkerns, overpyrite (euhedral); CaC03 concentrations

CaC0 3 concretionary mud steinkerns; minor overpyrite

Phosphatic and/or glauconitic steinkerns, often reworked; rare overpyrite

Dysaerobic­ anaerobic (euxinic) O2 < 0 . 3 mlll

Anoxic-surface; commonly organic-rich (commonly sulphidic)

No fillings : minor pyritic replacement; rarely, traces of soft parts

Mud steinkerns; pyrite patinas; periostracal remnants

Highly compacted mud steinkerns

=

oxygenation of the lower water column and upper sediments (Tables 1, 2; Brett & Baird 1986) . The concept of taphofacies has been applied recently to the subdivision and interpretation of ancient sedimentary environments . For example, Speyer & Brett (1986) used a combination of quali­ tative observations and semiquantitative indices of . preservation in widespread phacopid trilobites to recognize nine distinctive taphofacies in the Middle Devonian Hamilton Group of New York State (Fig. 1 ) . Preservation indices included relative frequency of fragmentation, up-and-down orientations of concavo-convex skeletal parts, cephalon- pygidium ratios, percentage of articulated trilobites and moult remains, and percentage of enrolled versus out­ stretched individuals . The taphofacies recognized display a broad range of preservational grades . Taphofacies 1 i s characterized b y almost completely disarticulated, sorted and highly fragmented trilo­ bite remains, which are indicative of low rates of deposition in high-energy environments. In contrast Taphofacies 3 and 4 display high proportions of complete outstretched skeletons, or moult assem­ blages. In addition to biostratinomic characteristics, observations on early diagenetic minerals in the fossil trilobites were analysed and used in the inter­ pretation of sediment geochemistry and oxygenation. For example, abundant pyrite was found to be associated with other evidence for dysaerobic but not anoxic settings, where moderate rates of sedi-

mentation prevailed (Fig. 2) . Similarly, Fisher and Hudson (1987) compared pyrite geochemistry and fossil preservation in ammonoid shells and dis­ tinguished three taphonomically separate groups of fossil assemblages from the Jurassic Oxford Clay of Britain. Flattened, highly compressed ammonites with very minor pyrite are typical of black shale environments, in which relatively weak gradients existed between organic remains and their sur­ rounding sediments; in contrast, grey bioturbated facies provided excellently preserved, uncompacted pyrite steinkerns of fossils (see also Section 3 . 7) . A similar approach i s illustrated by Martill's (1985) study of modes of preservation in marine ver­ tebrates, also from the Oxford Clay of the U.K. He was able to distinguish five distinct types of preser­ vation among crocodilians, ichthyosaurs, and fish; these included completely articulated to variously disarticulated skeletal remains, isolated bones and teeth, worn bones, and coprolitic accumulations . Martill observed a correlation between the organic content of the sediment and the degree of skeletal articulation, and noted trends in vertebrate preser­ vation throughout transgressive - regressive cycles that reflect variations in sedimentation rates . Norris (1986) and Flessa & Fiirsich (1987) recog­ nized gradients of taphonomic indices, such as fragmentation and abrasion, amongst Neogene molluscan assemblages . Taphonomic gradients were arrayed approximately perpendicular to the

260

3 Taphonomy Taphofacies 4C

Taphofacies 3 A

' Taphofacies 4A

Taphofacies 2 B

16V! Av

y

Taphofacies 4 B Fig. 1 Reconstructed panorama o f Hamilton Group (Middle Devonian, New York State) trilobite taphofacies and summary of taphonomic attributes . Disarticulation was mediated by current-related processes (C), surficial bioturbation (8s), and/or deep, intrastratal bioturbation (80); these agents are differentiated on the basis of scIerite orientation. Articulated remains are categorized according to body posture (0 outstretched, E enrolled) and mode of generation (M moult) . Taphofacies lA alld l B display modes of fossil preservation that indicate a taphonomic history involving long-term lag accumulation and deposit reworking in a nearshore setting. Taphofacies 2A alld 2B are characterized by pervasive Zoophycos­ like bioturbation and a relative abundance of enrolled corpses; sedimentation rate was moderately high and substratum was water saturated, well oxygenated, and easily suspended. Taphofacies 3A displays abundant disarticulated but non-fragmented remains; because of insignificant sediment supply, these accumulated to form thin, laterally persistent layers . Taphofacies 3B is characterized by prominent shell layers in which shell concentration was the result of sediment bypass; sediment was carried to and deposited in deeper-water settings . Taphofacies 4A reflects very low rates of sedimentation in deep, quiet water conditions; trilobite debris accumulated between depositional events and may have served as substrate for various sessile organisms. Taphofacies 4B indicates higher rates of sedimentation, probably as a result of bypass in more proximal environments (e .g. Taphofacies 38); sediment chemistry favoured early pyrite diagenesis, which indicates dysaerobic-anaerobic conditions . Taphofacies 4C represents very high sedimentation in a deep-water setting and is characterized by anaerobic sediment chemistry, low-diversity faunas, and an unstable substratum. Comparative taphonomic analysis enhances our perception of stratigraphic facies as dynamic environmental units that are distributed in an orderly fashion with respect to specific physico-chemical parameters. This reconstruction is a generalized synthesis of bathymetrically and sedimentologically related environments on the basis of observed taphonomic products and inferred sedimentary processes. (From Speyer & 8rett 1986. ) =

shore line, and reflected decreasing severity of re­ working events in an onshore direction for tidal flats (Flessa & Fiirsich 1987) and an offshore direc­ tion for a Miocene shelf (Norris 1986) . Speyer and Brett (1988) used a deductive approach to produce a hypothetical model of taphofacies for various environmental settings of ancient epeiric seas (Fig. 3) . Hypothetical distributions of tapho­ nomic properties, such as articulation ratio, convex

=

=

up-and-down orientations of shells, and relative degree of fragmentation and abrasion, were con­ toured along gradients of depth and sedimentation rates to produce generalized three-dimensional block diagrams (Fig. 3) . For example, disarticulation and fragmentation should be highest in areas where sedimentation rates are at a minimum and where the sea floor is continually reworked by current or wave disturbances . Optimal levels of articulation

261

3 . 9 Taphofacies Py r i t e Tap h o fac i e s M o d e l

I n u ndat i o n - d i l u t i o n

c

.9

1§ c
E

"1J
�

en

u c

O x i d at i o n

C o n d e n sat i o n I n c reas i n g Oxygen Ove r l y i n g Wate r : S ed i m e n t :

Anae rob i c Anoxic

Dysae ro b i c

Aerobic Oxic

Schematic diagram illustrating the range of conditions that favour formation of various forms of early diagenetic pyrite (see also Section 3 . 8 .3). Note that pyrite formation is enhanced in sulphidic microenvironments, within nonsulphidic sediments, and with moderate sedimentation rates. Little or no concentration gradient exists in anaerobic, organic-rich (sulphidic) muds, while fully aerobic conditions in the upper sediment clearly militate against pyrite formation. Organic matter must be buried in sediment to initiate bacterial action; however, too high a rate of deposition will swamp early diagenetic reactions by diluting the necessary concentrations . (After Brett & Baird 1986 . ) Fig. 2

and minimal fragmentation would occur in low­ energy environments with high sedimentation rates. Trends in the frequency or percentage of event deposits (such as storm-generated shell layers) can also be contoured using a similar diagram and provide an additional type of taphonomic data which can be used in interpreting ancient facies . Synthesizing these simple deductions, it was possible to construct taphofacies models (Fig. 4)

which approximate distribution patterns of tapho­ facies observed in empirical studies (e . g . Speyer & Brett 1986) . The concept of taphofacies requires further testing in many modern marine settings, as well as in various ancient depositional environments . How­ ever, if taphofacies can be recognized consistently, it should be possible to reconstruct patterns of ancient sedimentation rates and other factors,

3 Taphonomy

262

Con cavo-convex O r i e n tat i o n s Degree of S o rt i n g

Deg ree of D i sa rticu lation

LOW

•

Few Foss i l s Present

Degree of F ragm e n tat i o n

Degree of Corras i o n

HIGH

VERY/-fIC) /

LO W

�

c

Fig. 3. Biostratinomic gradients with respect to three generally defined environmental parameters: sedimentation rate (decreases right to left); turbulence (i . e . current energy, decreases downslope from top to bottom); sea-floor oxygen (decreases downslope - oxic, dysoxic, anoxic) . Duration of surface exposure is inversely proportional to sedimentation rate and is important in regulating the magnitude of illustrated taphonomic properties . A Abrasion, C Corrosion. =

and hence to refine interpretations of ancient sedimentary environments .

References Brett, C . E . & Baird, G . c . 1986 . Comparative taphonomy: a key to paleoenvironmental interpretation based on fossil preservation. Palaios 1, 207- 227. Fisher, 1. St. J. & Hudson, J . D . 1987. Pyrite formation in Jurassic shales of contrasting biofacies . In: J. Brooks & A.J. Fleet (eds) Marine petroleum source rocks, pp. 69 - 78.

=

Special Publication of the Geological Society of London, No. 24 . Flessa, K.W. & Fiirsich, F.T. 1987. Taphonomy of tidal flat molluscs in the northern Gulf of California: paleoenvi­ ronmental analysis despite the perils of preservation. Palaios 2, 543- 559. Martill, D.M. 1985 . The preservation of marine vertebrates in the Lower Oxford Clay Ourassic) of central England .

Philosophical Transactions of the Royal Society of London, B311, 155 - 1 65. Norris, R.D. 1986. Taphonomic gradients in shelf fossil assemblages : Pliocene Purisima Formation, California. Palaios 1, 256- 270.

3 . 1 0 Plant Preservation TAP H O FAC l E S

263

1 High

H igh

Low

o

Low

S e d i m e n ta t i o n RlS

C

F

H igh TAPH O FAC I ES

o

RlS

F

C

TAP H O FAC I E S

H ig h

4 TAP H O FAC I E S

Low

o

TAP H O FAC I ES RlS

5

F

C

Low

o RlS

6

Low

o RlS

F

7

C

C

Fig. 4 General taphofacies for Palaeozoic epeiric seas . Seven distinct taphofacies are recognized on the basis of differences in four taphonomic properties: D disarticulation, RlS reorientation and sorting, F fragmentation, C corrasion, i . e . corrosion/abrasion. These seven taphofacies, in turn, reflect environmental conditions i n corresponding fields o f the general block diagram . Environmental conditions are coarsely represented by the three indicated parameters (sedimentation rate, turbulence, and oxygenation) . (From Speyer & Brett 1988 . ) =

=

Speyer, S . E . & Brett, C . E . 1986. Trilobite taphonomy and Middle Devonian taphofacies . Palaios 1, 312 - 327.

=

=

Speyer, S . E . & Brett, c . E . 1988 . Taphofacies models for epeiric sea environments: Middle Paleozoic examples. Palaeogeo­ graphy, Palaeoclimatology, Palaeoecology 63, 225 -262 .

3 . 10 Anatomical Preservation of Fossil Plants A . C . SCOTT

Introduction

Plant fossils may be preserved: (1) as compressions; (2) anatomically, as fusain (fossil charcoal) where the cell walls have been converted to pure carbon by fire; and (3) as permineralizations, where original

cell walls are still preserved, or as petrifactions, where cell walls have also been replaced (usually by silica, carbonate, or pyrite) . While compressions are both common and useful, they preserve no internal structure, and it is anatomically preserved plants that provide most data (Fig. 1 ) .

264

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3 Taphonomy O rgan i c ce l l wa l l

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F Fig. 1 Anatomical preservation of fossil plants . A, wood (plant cells lacking living contents) . B, Detail of transverse section showing cell walls. C, compression with the closure of cell lumina . D, Conversion of cell wall to almost pure carbon by fire (charcoal). E, Early infiltration of cell lumina by permineralizing fluids with crystallization of calcite, silica, or pyrite (giving cell internal moulds) . F, Decay of organic cell walls and secondary crystallization of calcite, silica, or pyrite to produce a petrification (giving casts of cell walls) . (After Scott & Collinson 1983 . )

Fusain

By far the most widely distributed anatomical mode of plant preservation, both geographically and stratigraphically, is fusain . It occurs widely in post­ Silurian sediments (Scott & Collinson 1978) . During burning, the cell walls are converted to pure carbon and above 300°C the middle lamella of the cell is homogenized with the rest of the cell wall (Cope & Chaloner 1985) (Fig. 2F) . The cellular structure is beautifully preserved and may be studied particu­ larly well by scanning electron microscopy (Fig. 2D, E); being pure carbon the cell walls are resistant to bacterial decay and acquire rigidity . Many smaller plant parts, including not only leaves and fruits but also delicate flowers, have been preserved in this way. Only larger plant organs break up during burning and because of physical damage during transport. Several important plants, including Cretaceous flowers and the earliest Carboniferous conifers, are preserved as fusain (Scott 1989) .

Permineralization is where the cell spaces are infil­ trated by mineral-rich solutions and precipitation takes place (Fig . lE), preserving the organic cell walls (Schopf 1975) . The most common precipitating mineral is calcium carbonate, followed by silica and pyrite . Calcareous permineralization is best known from the Upper Carboniferous coal balls of Europe and North America (Fig. 2B), but coal balls are also known from the Permian of China . Coal balls are limestone concretions encountered in coal seams, and are permineralized peat (Scott & Rex 1985) . Calcium and magnesium carbonate infiltrated the peat before significant decay or compaction took place (see also Section 3 . 8 .2), giving an exceptionally preserved fossil plant assemblage . Coal balls preserve fine anatomical and histological details and even cell contents such as starch grains, nuclei, germinating spores, gametophytes, pollen drops, pollen tubes and plant apices . Several hypotheses have been put forward to explain the occurrence of coal balls but the presence of marine bands over­ lying the coal seams strongly suggests a marine influence . The calcite is precipitated as radiating fibrous crystals which nucleate on cell walls (Scott & Rex 1985) . Coal balls may occur singly and in rare cases may nearly replace a seam. Palaeoecological studies have identified changing plant communities in vertical profiles of coal balls through a seam . Calcareous permineralizations may be found in a wide range of environments, including marine rocks, freshwater mudstones, siltstones, and sand­ stones (Fig. 2C), and are also commonly associated with basaltic volcanic rocks . Basaltic ashes often yield abundant anatomically preserved plants . Here the calcite was probably released from the break­ down of various minerals in the ashes . Some of the most famous anatomically preserved plants are permineralized by silica (Knoll 1985; see also Section 1 .2) . The silica is usually the product of volcanic activity, but in rare cases silica permineral­ izations are found in marine radiolarian cherts . Both peats (Fig. 2A) and individual plants may be preserved in this manner and the Early Devonian Rhynie chert is a good example . Occasionally, upright trunks in fossil forests are preserved, such as the Purbeck fossil forest in southern England . Often the original cell walls are also replaced in minute detail by a second gener­ ation of silica, forming a true petrification where no organic material remains (Schopf 1975) (Fig. IF) . The Triassic Arizona fossil forest and that from

3 . 1 0 Plant Preservation

265

Anatomically preserved fossil plants . A, Siliceous permineralized and partly petrified peat ( x 1) composed mainly of the seed plant Glossopteris with branches showing growth rings and its roots (Vertebraria) . Permian, Bowen Basin, Australia. (From Collinson & Scott 1987.) B, Carboniferous coal ball ( x 2). Calcareous permineralized peat showing pteridosperm and fern axis with stigmarian rootlets, Westphalian A, Lancashire. (From Scott & Rex 1985 . ) C, Calcareous permineralization of pteridosperm stem, Stenomyelon tuedianum ( x 10) from non-marine calcareous sandstone, Lower Carboniferous, Scotland. D, Scanning electron micrograph of fusainized leaf of the Lower Cretaceous fern Weichselia ( x 30) from the Isle of Wight, U.K. E, Scanning electron micrograph of fusainized xylem cylinder of the herbaceous lycopod Oxroadia ( x 10) from the Lower Carboniferous of Donegal, Ireland . (From Scott & Collinson 1978 . ) F, Scanning electron micrograph of modern beech charcoal (Fagus) after a man­ made fire on Box Hill , Surrey, showing fine preservation of vessel-to-vessel pitting ( x 200) . Fig. 2

3 Taphonomy

266

Yellowstone National Park (Tertiary) are good examples of this type of preservation . Plant compressions often show partial perminer­ alization by pyrite . Pyrite may form in stagnant conditions and is often associated with bacterial activity (see also Section 3 . 8 . 3) . It may fill cell spaces and often occurs as framboids . In many cases several generations of pyrite are present which have infil­ trated spaces left by decaying organic material . Complex casts and moulds of cell walls may be produced and may be difficult to interpret (Grierson 1976) . In some cases the pyrite has been converted to limonite . Permineralized plant com­ pressions are especially useful as they provide data on both morphology and anatomy. References Collinson, M . E . & Scott, A . c . 1987. Implications of veg­ etational change through the geological record on models of coal-forming environments. In: A . C . Scott (ed . ) Coal and coal bearing strata: recent advances. Special Publication of the Geological Society of London, No. 32, pp . 67-85. Blackwell Scientific Publications, Oxford.

Cope, M.J. & Chaloner, W . G . 1985 . Wildfire : an interaction of biological and physical processes . In : B. Tiffney (ed . ) Geological factors and the evolution of plants, pp. 257-277. Yale University Press, New Haven . Grierson, J . D . 1976 . Leclercqia complexa (Lycopsida, Middle Devonian) : its anatomy and the interpretation of pyrite petrifactions. American Journal of Botany 63, 1 184- 1202. Knoll, A . H . 1985 . Exceptional preservation of photosynthetic organisms in silicified carbonates and silicified peats .

Philosophical Transactions of the Royal Society of London B311, I 1 1 - 122. Schopf, J . M . 1975 . Modes of fossil preservation. Review of Palaeobotany and Palynology 20, 27-53. ScoU, A.C. 1989 . Observations on the nature and origin of fusain. International Journal of Coal Geology 12, 443 -475 . Scott, A . C . & Collinson, M . E . 1978 . Organic sedimentary particles : results from scanning electron microscope studies of fragmentary plant material. In: W . B . Whalley (ed. ) SEM in the study of sediments, pp. 137- 167. Geo­ abstracts, Norwich . ScoU, A . C . & Collinson, M . E . 1983 . Investigating fossil plant beds. Part I: the origin of fossil plants and their sediments. Geology Teaching 7, 114- 122 . ScoU, A . c . & Rex, G . M . 1985 . The formation and significance of Carboniferous coal balls. Philosophical Transactions of the Royal Society of London B311, 123- 137.

3 . 11 Taphonomy of Fossil-LagersHitten

3 . 11 . 1 Overview A . SEILACHER

Terminology and goals

The term 'Fossil-Lagerstatten' (singular Lagerstatte) is derived from the German mining tradition . 'Lagerstatte' is any rock or sedimentary body con­ taining constituents of economic interest. Accord­ ingly, a Fossil-Lagerstatte is any rock containing fossils which are sufficiently well preserved and/or abundant to warrant exploitation - if only for scientific purposes . The problem with this term is that it defines no boundary. Just as low-grade min­ eral deposits may become economic as market prices rise, so almost any fossiliferous rock may rise to the level of distinction in the eyes of an inquisitive researcher.

What matters here is the concept behind the term. Basically, the preservation of any fossil is an exceptional event that deserves our attention. As Raup and Stanley (1978) pointed out, a single square metre of sea floor could, during a few million years, produce enough shells to swamp the museums of the world, were all of them to be preserved . Also the calcium budget of the ocean would rapidly collapse without taphonomic recycling. Since, however, we cannot hope to solve the case history of every single fossil, our attention focuses on occurrences that are extraordinary by geological standards . Nevertheless, we should not treat them as a separate class of rocks, but as end members of related groups of sedimentary facies, different only in that their additional palaeontological information may reveal interesting details about the environ­ mental, depositional, and diagenetic history of the whole guild . Admittedly, this has not always been the view of collectors . Well preserved fossils have an attraction of their own and may reveal new

3 . 1 1 Fossil-Lagerstiitten palaeobiological details in isolation from their geo­ logical context. However, as in archaeology, con­ trolled excavation methods are gradually replacing the old treasure-hunting approach. Given that preservation is not random, extra­ ordinary fossil occurrences (the term 'biota' should be avoided when considering taphonomic conditions) should fall into genetic groups, defined with reference to typical examples . In the classifi­ cation outlined in Fig. 1, concentration deposits and conservation deposits are distinguished as main categories (see also Seilacher et al. 1985) . They are discussed below, proceeding from the more normal to the extreme cases. Concentration deposits

Of the two main categories, concentration Lagerstiitten are the less spectacular group because the quality of individual preservation may not be extraordinary in any way. But preservation is unusual not only if soft parts are preserved; the episodic prevention of hard part recycling may be just as noteworthy. For example, to explain the common coquinas, in which the shells of gastropods, burrowing bivalves, or ammonites have accumulated, as representing periods during which the particular community thrived more than usual would be unrealistic. All three mollusc groups have aragonitic shells, which are chemically unstable and would have been destroyed by the combined action of shell borers, algae-nibblers, and dissolution, had they been lying unprotected on the sea floor for thousands of years (see also Sections 3 . 3, 3 . 8 . 1 ) . In a famous ammonite coquina in the Middle Jurassic of the Normandy coast, the shells are so perfectly preserved that they still have a nacreous lustre (Fiirsich 1971 ) . Yet the decimetric bed contains a mixture of ammonites from two stratigraphic zones representing c. 2 million years! A combination of two processes was therefore required: (1) sedi­ mentation to seal the shells, before they could become corroded, in a well buffered and non-cementing sediment; and (2) one or a few concentration and mixing events brief and gentle enough not to destroy the delicate shells . These contradictory conditions are met in mud bottoms below normal storm wave base, when sedimentation rate is reduced by trans­ gression . But the site still had to be within reach of the effects of the few largest storms (in two million years!) that did the mixing and concentration by winnowing away the finest fraction, yet deposited enough mud on top of the tempestite to provide

267

a new seal. The association of these Normandy ammonites with large bivalves (Ctenostreon) is also important. Their thick valves and outriggers indi­ cate that they were passive recliners on muddier sediments than are now preserved. But they also indicate that sedimentation rates were low and storms rare enough to allow such a lifestyle . Another common class of multiple-event coquinas are oyster beds (Seilacher 1985) . Significantly they consist always of reclining or mud-sticking soft bottom species . Since oysters have calcitic shells, it is probable that the embedding sediment was more corrosive than in the previous case and eliminated the aragonitic shells that should normally have been found in association. Also revealing is the accumu­ lation of such oysters into mounds . It shows that the storm reworking involved little transport, so that preferred sites could grow up like Meso­ potamian tells in spite of periodic destruction. Still another kind of storm coquinas are bone beds, which commonly occur in the final stages of larger regression cycles (the Silurian of Ludlow; top of the German Muschelkalk), or in the initial trans­ gression . Here an unusual concentration of phos­ phatic vertebrate remains occurs, usually in a matrix of coarse sand or small lithoclasts . The idea of a mass mortality (as during red tides) would again be misleading, because, along with teeth and ganoid fish scales, there is a high concentration of copro­ lites. Some of them, as well as the few associated bones, show ancient fracture surfaces that are angular - different from the way the fresh objects would have broken. In this case the biomaterials were not only sealed in the sediment between reworking events, but also became preJossilized by early phosphatization (Section 3 . 8 .4) . This indicates that the original host muds were anoxic - although no sedimentary clues to this survived the final storm. This theme extends to include coquinas made up of crinoid remains (originally consisting of high magnesium calcite stereom that may become pre­ fossilized into more stable calcite and into massive crystals), or to brachiopod and trilobite coquinas . In all cases early diagenesis is likely to have played a role, but also to have considerably distorted the original spectrum of the fauna (see also Section 3 . 8 . 1 ) . Nevertheless, such beds provide us with valuable information about sedimentary regimes, both in the background facies and during perturbation events . Not all concentration deposits are stratiform. In terrestrial, but also in marine environments, we

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may find local concentrations of fossils in protected cavities - varying in size from body chambers of ammonite shells to fissures and caves. Such concentration traps provide primarily mechanical protection, but they may also shield their contents from diagenetic dissolution, either by inducing early concretion formation or by buffering the pore­ water. Conservation deposits

In this case it is not the quantity but the individual quality of preservation that matters (see following sections) . Some of the most famous conservation deposits (e . g . Solnhofen; Section 3 . 1 1 .7) are in fact rather barren. To appreciate what is going on, we must consider some of the processes that cause unusual preservation .

Preservation processes. Normally, carcasses quickly decompose through the activities of scavengers and microbes . As a result, soft parts are lost and composite skeletons disarticulate . But also the organic components of the skeletal parts (bone collagen, periostracal coating of mollusc shells, chitin of arthropod cuticles; lignin and cellulose in plants) will eventually be consumed by microbes . The incompleteness of this biological recycling (necrolysis; Section 3 . 1) is what makes for unusual preservation . Causes vary from case to case, but they encompass all the methods that humans use to keep their food from decomposing: in the Pleistocene, mammoth carcasses were deep-frozen in clefts in the glacial permafrost of Siberia, while a contemporary woolly rhinoceros in Galicia became pickled in a salty oil swamp, and ground sloths in South American desert caves were mummified by desiccation . On a smaller scale, Tertiary insects became sealed in resin that matured into amber (Section 3 . 1 1 .9) a material whose low density allows for secondary concentration into sedimentary placers . Other insect remains were saved from destruction by being en­ closed in the excrement of their consumers. In low oxygen lithotopes this matrix was prone to early bacterial phosphatization . Since the resulting coprolites are heavier than ordinary sedimentary particles, they again tend to form secondary placers, which facilitate the search for insects in them. Bacteria, however, may also be a positive factor. They were probably responsible for the selective phosphatization of small chitinous arthropods in the Cambrian 'Orsten' (Section 3 . 1 1 .3), which can

be freed from their calcareous matrix by etching, without damage even to the fine setae . A similar interaction appears to be involved in the preservation of vertebrate skin contours of aquatic vertebrates (Wuttke 1983) . Bacterial pyritization is another pro­ cess that may selectively preserve small arthropods, although this process is more familiar in ammonites, whose empty chambers became lined with fram­ boidal pyrite before the aragonitic shell was dissolved. The examples cited so far reflect localized pre­ servational conditions, which could be grouped as conservation traps . In contrast, stratiform conser­ vation deposits comprise larger rock units in which incomplete necrolysis was a general phenomenon. Although local microenvironments and bacterial interactions are by no means excluded, these strati­ form deposits call for larger scale causes, of which sediment smothering (obrution; Section 3 . 6) and anoxic conditions (stagnation) in the water column are most prevalent. In most instances both factors are involved, but the dominance of one or the other makes a great difference with respect to the ecologi­ cal spectrum preserved . Therefore, the separation of obrution and stagnation deposits is well justified, however ambiguous it may be in particular cases .

Obrution deposits . I n principle, smothering (Sec­ tion 3 . 6) is an episodic process that affects mainly bottom-living organisms . But it is selective not only in an ecological sense, but also taxonomically . This is because some groups of animals are, by virtue of their general organization, more vulnerable to such catastrophes . Such a group are the echinoderms, probably because their ambulacral system com­ municates with the ambient seawater and becomes easily clogged by fine sediment . This means that sudden mud sedimentation can kill and preserve the victims simultaneously . A classic example of echinoderm obrution is found in southern Germany at the very base of the Jurassic transgression (Rosenkranz 1971 ) . Except for a few small oysters, the perfectly preserved thanatocoenosis contains exclusively echinoderms, in spite of different life styles : predatory starfish, scavenging brittle stars, grazing echinoids, and filter-feeding stalked crinoids . Their burial at the top of a thin basal conglomerate and below a deci­ metre layer of dark shale is significant. It indicates that a local hard bottom fauna (probably also con­ taining members of other, less vulnerable phyla) was hit by a storm-generated mud fall . It is also possible that the change in sedimentation coincided

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3 . 1 1 Fossil-Lagerstiitten

N O N-MAR I N E C O N C E NTRAT I O N D E PO S ITS C o n d e n sa t i o n deposits Placer deposits Concentration traps

MAR I N E

D

H>HJ _

C O N S E RVAT I O N D E PO S ITS Stag n a t i o n deposits O b ru t i o n deposits C o n s e rvat i o n traps

Fig.

1

-

Synopsis and classification of fossil-Lagerstatten. (After Seilacher et a/ . 1985 . )

with a drop in local oxygen levels, because extensive bioturbation would otherwise have jumbled the buried echinoderm skeletons afterwards . Obrutional echinoderm layers are known from many epicontinental carbonate basins (see also Section 3 . 6) . They are always located between the coarser and the muddy phase of storm layers, but it is the amalgamated rather than the single-event tempestites in which they are most commonly found . To cite another example from southern Germany, the crinoid beds of the Upper Muschelkalk are particularly telling. Here the bed itself is a typical crinoid coquina representing the dissociated ossicles of many crinoid generations that flourished during a long interval of starved sedimentation. But it was only the terminal storm and the onset of heavier mud sedimentation that left an obrution deposit of perfectly preserved crinoids on top of the coquina of earlier populations . Echinoderm layers are also common in the Palaeozoic, whereas in other settings trilobites appear to have been a similarly vulnerable group (Section 3 . 6) . A more complex example of obrution i s the Hunsriick Slate (Hunsriickschiefer) (Section 3 . 1 1 .4) . Lithologically the slates resemble black shales. They also preserve non-mineralized arthro­ pod cuticles; but largely through pyritization

(probably bacteria-mediated), which is absent in truly anoxic shales . On the other hand, the Hunsriick Slate contains trace fossils and other remains of a rather diversified autochthonous bottom fauna. Still, as in other obrution deposits, echinoderms are overrepresented . Even more ambiguous is the dark-coloured Burgess Shale (Section 3 . 1 1 . 2), because in this case there are no trace fossils to attest to an autochthon­ ous bottom fauna. Still, most of the well preserved soft-bodied organisms, as well as the trilobites, were probably benthic, while their perfect preser­ vation indicates low oxygen levels at the place of their burial . This brings the Burgess Shale geneti­ cally close to the lithographic limestones of Solnhofen discussed below .

Stagnation deposits. While anoxia is usually associ­ ated with black, bituminous sediments, the famous lithographic limestones (Solnhofen; Section 3 . 1 1 . 7), however, may be cited as a striking counter­ example . In spite of being very pure (and now white) limestones, they contain a predominantly water- and airborne fauna in perfect preservation. Traces do occur, but (except in better aerated mar­ ginal zones) they were produced by benthic organ­ isms which were swept into the deeper abenthic

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3 Taphonomy

zone and died at the ends of their trackways . It is also remarkable that not only Archaeopteryx, but also fish skeletons show a characteristic dorsal cur­ vature of the vertebral column . This phenomenon typically occurs in carcasses dried out on land . It could also have resulted from dehydration in a brine, which in this case might have been the reason for a stratified water column and anoxia in the basin centre . Similar lithographic limestones are known from other geological levels . While showing varying pre­ servational histories, most of them are associated with relatively small depressions formed by reef growth (e .g. Triassic, Alcover; Hemleben & Freels 1977), tectonic pull-apart (Cretaceous, Lebanon; Hiickel 1970), or other processes (Hemleben 1977) . Bituminous shales, in contrast, may occur over very large areas, indicating that they needed vertical rather than lateral sediment supply. The Upper Liassic Posidonienschiefer (Holzmaden; Section 3 . 1 1 . 6) was laid down in an area covering large parts of Europe . Here the fauna is again predominantly pelagic. In contrast to Solnhofen, however, we occasionally find individual bedding planes covered by benthic fossils, whose perfect preservation (bivalves with the two valves still articulated in the butterfly position; echinoids with spines attached) indicates autochthonous burial - as in obrution deposits. These benthic events were originally thought to correspond to short phases of higher oxygenation . Savrda & Bottjer (1987; Section 4 . 19 .4) suggested that they represent an epibenthic window that opened every time the system passed from dysaerobic through 'exaerobic' to anaerobic con­ ditions, or vice versa. The probable reason is that under dysaerobic conditions, bioturbation produced a fuzzy interface and a nephel­ oid layer adverse to epibenthic life . As soon as bioturbation stopped, biomats could make the mud habitable for epibenthic specialists that either grazed on the bacteria or used them for chemosym­ biosis before oxygen levels became once again too low . Taphonomy, however, goes beyond necrolysis of soft parts and the sedimentological fate of the hard parts, to include diagenesis . Solnhofen and Holzmaden share a preservational history of am­ monite shells that differs significantly from dia­ genetic pathways in either limestones or dark shales, to which either example is more closely related in a lithological sense . In conclusion, the comparative palaeoecology and taphonomy of Fossil-Lagerstatten is a promising

field of research, but one in which palaeobiology has to be linked with other disciplines, such as sedimentology, geochemistry, marine biology, and - last but not least - actuopalaeontology. References Fiirsich, F.T. 1971 . Hartgrunde und Kondensation im Dogger von Calvados . Neues Jahrbuch for Geologie und Paliion­ tologie, Abhandlungen 138, 313-342 . Hemleben, C . 1977. Rote Tiden und die oberkretazischen Plattenkalke im Libanon. Neues Jahrbuch for Geologie und Paliiontologie, Monatshefte 1977, 239 -255. Hemleben, Ch. & Freels, D . 1977. Fossilfiihrende dolomitisierte Platten-Kalke aus dem 'Muschelkalk Superior' bei Montral (Prov. Tarragona, Spanien) . Neues Jahrbuch for Geologie und Paliiontologie, Abhandlungen 1 54, 186-212. Hiickel, U. 1970 . Die Fischschiefer von Haqel und Hjoula in der Oberkreide des Libanon. Neues Jahrbuch for Geologie und Paliiontologie, Abhandlungen 135, 1 1 3 - 149 . Raup, D . M . & Stanley, S . M . 1978 . Principles of paleontology. 2nd edn . Freeman, San Francisco . Rosenkranz, D . 1971 . Ziir Sedimentologie und Okologie von Echinodermen - Lagerstatten. Neues Jahrbuch for Geologie und Paliiontologie, Abhandlungen 138, 221 - 258 . Savrda, C . E . & Bottjer, D.]. 1987. The exaerobic zone, a new oxygen-deficient marine biofacies . Nature 327, 54- 56 . Seilacher, A. 1985 . The Jeram model: event condensation i n a modern intertidal environment. In: U. Bayer & A. Seilacher (ed . ) Sedimentary and evolutionary cycles . Lecture Notes in Earth Sciences No . 1, pp. 336 - 342 . Springer-Verlag, Berlin. Seilacher, A . , Reif, W-E . & Westphal, F. 1985 . Sedimen­ tological, ecological and temporal patterns of fossil Lagerstatten . Philosophical Transactions of the Royal Society of London B311, 5 -23. Wuttke, M. 1983 . 'Weichteilerhaltung' durch lithifizierte Mikroorganismen bei mittel-eozanen Vertebraten aus den Olschiefern der 'Grube Messel' bei Darmstadt. Senckenbergiana Lethaea 64, 509- 527.

3 . 11 . 2 Burgess Shale S . C ONWAY M O RRIS

Introduction

Study of the soft-bodied biota of the Middle Cambrian Burgess Shale has opened a unique window into Cambrian life, providing new insights into the nature of the major adaptive radiations amongst metazoans, the relative im­ portance of shelly taxa, and the role of different

3 . 1 1 Fossil-Lagerstatten trophic groups in the palaeoecology of early com­ munities (Whittington 1985; Conway Morris 1989; see also Section 1 .5) . As originally exploited by C. Walcott between 1910 and 1921, the fossils came from two quarries on the west slope of a ridge that connects Wapta Mountain and Mount Field, near the town of Field, British Columbia. These exca­ vations are in the basinal shales of the Stephen Formation, and the term 'Burgess Shale' is one of only local significance . The lower Walcott Quarry, exposing the so-called Phyllopod bed, has been by far the most prolific source of fossils, yielding over 65 000 specimens (Conway Morris 1986) . The higher, known as the Raymond Quarry, has been less productive but it provides a distinct assemblage distinguished by a lower diversity and different proportions of taxa in comparison with the Phyllopod bed. In addition, recent searches for comparable soft-bodied biotas elsewhere have yielded a rich harvest. In the vicinity of the Burgess Shale many new localities have been found . More importantly, discoveries elsewhere in the U . S . A . , Greenland, and south China have led to a realization that there is a distinctive Burgess Shale-type fauna with a specific and recurrent cha­ racter that ranges through the Lower and Middle Cambrian. However, in terms of taphonomic information little is yet known about most of these deposits, and existing insights depend largely on studies of the Phyllopod bed. All the occurrences of Burgess Shale-type biotas share the character of burial in fine-grained sediment, often in catastrophic cir­ cumstances, but it would be unwise to assume that their taphonomic histories were similar. Biota and sedimentary environment

Although studies of the Phyllopod bed biota, which includes both a benthic and pelagic fauna together with associated algae, are not complete, existing estimates of both the number of taxa and individuals (Conway Morris 1986) (Fig. 1) probably will not require radical revision. The benthic fauna (see Conway Morris 1979, 1986; Whittington 1985) is dominated by arthropods, of which only a small fraction are trilobites . In addition, other major groups include priapulid and polychaete worms, cnidarians, sponges, molluscs, echinoderms, and a variety of groups of uncertain taxonomic position (Conway Morris & Whittington 1985; Whittington 1985) . As might be expected, the fauna is dominated by relatively few taxa, some nine species accounting

271

for about 90% of the total . The pelagic fauna is identified largely on adaptations suitable for either a planktic or nektic existence, such as prominent fins, streamlined bodies, or abundance of gelatinous tissue (Conway Morris 1979) . In the Phyllopod bed there is strong evidence that much of the biota owes its preservation to catastrophic burial, including occurrence in graded beds, variable orientation of specimens relative to the bedding plane, and see­ page of sediment between appendages or other extensions of the body. Because the laminations of the Phyllopod bed lack disturbance or other evi­ dence of bioturbation, it is concluded that the en­ vironment of deposition was inimical to metazoan life, and this is confirmed by the exquisite preser­ vation. The excluding factor was most probably anoxic conditions with H2S, and an alternative possibility of hypersaline waters seems less likely because the specimens do not show obvious osmotic shrinkage or swelling. The biota clearly lived elsewhere, because it was transported into a hostile environment, and it is useful to recognize this pre-slide environment (Conway Morris 1986) . Its exact location is con­ jectural, but it is probably significant that all the soft-bodied localities in the Step hen Formation, in­ cluding the Phyllopod bed, were deposited in rela­ tively deep water immediately adjacent to an enormous carbonate bank which rose vertically and acted as a rim to extensive carbonate shoals and lagoons that extended hundreds of kilometres to the east. There is no evidence that any substantial frac­ tion of the biota was derived from the reef top or margins, and it is likely that the pre-slide environ­ ment was also adjacent to the reef base . There is also some evidence that the distance of transport between pre- and post-slide environments was relatively small, perhaps a kilometre or so. This figure is based on inferences of local palaeotopo­ graphy, inferred position of the photic zone relative to the post-slide environment, and survival of par­ tially decayed specimens whose delicate nature could survive only limited transport. Taphonomic history

The taphonomic history of the Phyllopod bed biota began, therefore, with the failure of the sea bed and its descent towards the post-slide environment. The area of sea floor may have been small, and additional specimens may have been trapped en route. As the flows were probably rather weak, extensive erosion and scouring out of the infauna

3 Taphonomy

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1 Frequency distribution of the 93 species that contribute to the benthic community of the Phyllopod bed . Note characteristic 'hollow curve' distribution, and also breaks in scale of ordinate . Inset histograms show relative percentages of the major groups in the Phyllopod bed. A, Genera . B, Individuals, alive and dead (i. e. empty exuviae) . C, Individuals alive at the time of burial . D, Estimated biovolumes. Stippled zone in arthropod column represents proportion of trilobites . Fig.

3 . 1 1 Fossil-Lagerstiitten seems unlikely, but addition of epifauna and pelagic elements that had strayed close to the sea bed probably occurred . However, other pelagic elements may have descended into the post-slide environ­ ment, and there is little doubt that the sampling of this assemblage is very incomplete . An important principle is that although the benthic flows contained many specimens alive at the time of transport, it also carried a cargo of resistant skeletal parts that had either been dis­ carded (e . g . by ecdysis in trilobites) or remained on death (e .g. in brachiopods, monoplacophorans, and hyoliths) . If an accurate census of the original living community is to be undertaken, it is, of course, necessary to subtract these exuviae and empty shells from the specimen totals (Conway Morris 1986) . In the case of hyoliths, with attached opercula and helens, and some inarticulate brachiopods with mantle setae extending beyond the valve margins, it is possible to establish whether the individual had been alive at the time of burial. In other cases, such as the monoplacophorans, it is not possible to determine vitality . However, by making reasonable assumptions it can be shown that the shelly com­ ponent was an insignificant part of the living com­ munity, perhaps as little as 2% . Reasons for death are probably linked to arrival in the inhospitable post-slide environment, but it is likely that much of the fauna was either stunned or dying by the time of deposition. This is because animals placed in an anoxic environment often coil tightly as they enter a metabolic stasis; this feature has not been observed in the Phyllopod bed speci­ mens . Moreover, the lack of evidence for escape Fig. 2 Back-scattered electron micrographs of Burgess Shale fossils. A, Eldonia, surface with potassium mica (dark) and a coating of calcite (light), with a nodule of barium sulphate (very bright), x 65 . B, Transverse section of inarticulate brachiopod (Dictyollina) with original phosphatic shell and blades of potassium mica, x 125. C, Transverse section of trilobite (Olenoides) with exoskeleton partially replaced by pyrite (very bright) enclosing calcite (grey) and elsewhere silicates (light coloured chlorite and dark potassium mica), x 70 . D, The sponge Choia, surface showing spicules composed of silica and scattered nodules of cerium phosphate (very bright), X 160. (Photographs based on unpublished work with K. Pye . )

273

activity also supports the notion that the fauna was incapacitated during transport. In the post-slide environment the majority of specimens were buried, but occasional individuals that show scattering of parts may have lain on the sea floor, where they were disturbed by weak cur­ rents . After burial decay commenced, and this is best seen by a dark stain that surrounds an indivi­ dual and appears to represent body contents that oozed out into the sediment (Whittington 1985) . However, decay was evidently limited and, for reasons that are not understood, the processes of fossilization began.

Diagenesis. At present the soft parts of fossils are composed of carbon films (Butterfield 1990) coated by silicate films, principally chlorite and potassium micas (Fig. 2A) . In terms of the hard parts, those of calcareous organisms are replaced by similar sili­ cates, although in some cases pyritization has been extensive (Fig. 2C) . However, phosphatic species, including the inarticulate brachiopods (Fig. 2B), retain their original composition, while in some cases the sponges retain the siliceous composition of their spicules (Fig . 20) . In many soft-bodied Lagerstatten the role of bacteria is being realized now as a key step in exceptional preservation, es­ pecially in the form of coatings that may be subject to rapid mineralization . Although their role in phosphatization has received particular attention (Section 3 . 1 1 .2), recent work has shown how iron aluminium silicates can also arise during microbial activities (Ferris et al. 1987) . Fossilized bacteria are now widely known, but have not been recognized

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274

3 Taphonomy

in the Phyllopod bed, perhaps being obliterated during subsequent diagenesis . Indeed, the dia­ genetic alteration of the Burgess Shale has only received limited study, but in addition to the changes in the silicates, nodules of barium sulphate (Fig. 2A) and cerium phosphate (Fig. 2D) also formed. The taphonomic history of the Phyllopod bed continued with increasing depths of burial beneath substantial thicknesses of younger sediments . Thrust sheets (including the Cambrian sections with the Stephen Formation on the Simpson Pass thrust sheet) were propelled eastwards as part of a major orogeny during the Mesozoic to Early Cenozoic. Associated with these movements was the development of a strong penetrative cleavage in the argillaceous units . More basinal equivalents of the Stephen Formation were thus affected, and were it not for the massive dolomites of the Cathedral Escarpment providing a tectonic shadow zone, the soft-bodied localities adjacent to this reef would have also been deformed, making recovery of fossils impossible . The final stage of taphonomy, that of its discovery, is to the credit of Walcott, whose chance stumbling on this superb fauna has answered some questions, but set many more .

The. Upper Cambrian Alum Shale of southern Sweden first yielded small arthropods with pre­ served cuticular organs in 1975 . Since then, a large variety of such fossils has been recovered at 22 localities from at least five trilobite zones or sub­ zones. They have been discovered over a wide area in Northern and Central Europe, mainly in Vastergotland (Kinnekulle, Hunneberg, Falbygden), Skania, on the island of bland, in a borehole in northwestern Poland, as well as in drift boulders throughout northern Germany. The fine preser­ vation (Fig. 1) permits detailed comparison not only between the various 'Orsten' animals, but also with extant arthropod orders . Thus the material is im­ portant for considerations of the phylogeny of early arthropods and of the relationship between the Recent orders.

References

Sedimentary environment

Butterfield, N.J. 1990. Organic preservation of non-minera­ lizing organisms and the taphonomy of the Burgess Shale . Paleobiology 16, 272 � 286. Conway Morris, S . 1979 . The Burgess Shale (Middle Cambrian) fauna . Annual Review of Ecology and Systematics 10, 327� 349 . Conway Morris, S. 1986. The community structure of the Middle Cambrian Phyllopod bed (Burgess Shale). Palaeontology 2 9 , 423� 467. Conway Morris, S . 1989 . Burgess Shale faunas and the Cambrian explosion . Science 246, 339 � 346. Conway Morris, S. & Whittington, H . B . 1985. Fossils of the Burgess Shale . A national treasure in Yoho National Park, British Columbia. Report of the Geological Survey of Canada 43, 1 �31 . Ferris, F . G . , Fyfe, W . S . & Beveridge, T.J. 1987. Bacteria as nucleation sites for authigenic minerals in a metal­ contaminated lake sediment. Chemical Geology 63, 225 � 232 . Whittington, H . B . 1985 . The Burgess Shale. Yale University Press, New Haven.

'Orsten' is a sulphurous anthraconitic limestone, occurring either as concretions of about 0 . 1 - 2 . 0 m in diameter, or as large flat lenses within the Alum Shale, which may appear as beds in small outcrops . I t i s commonly banded, because o f the fossil layers containing an abundant and varied trilobite fauna represented mainly by exuvia, and/or because of an alternation of lighter, often more sparitic bands with darker, finer-grained ones . There is no appar­ ent difference in the composition of the fauna from either lithology. In general the limestone is rather carbonaceous and often petroliferous. When dis­ solving such a sample in acid, the oil usually con­ centrates on top of the liquid . Less carbonaceous beds are beige to light grey. Quartz grains are lacking in both the Alum Shale and the 'Orsten' . Most sediment deposition was under very low­ energy conditions. Finely dispersed pyrite indicates the absence of oxygen at the time of deposition. Higher energy sediments composed of fossil hash are rather limited and have not yielded specimens with preserved soft integument. There is an abundance of calcareous shelly re­ mains; phosphatic fossils are less frequent. Conodonts generally have a dark brown-blackish

3 . 1 1 . 3 Upper Cambrian 'Orsten' K . J . MUL L E R

Introduction

3 . 1 1 Fossil-Lagerstiitten

275

Fig. 1 Examples of 'Orsten' arthropods from the Upper Cambrian of Sweden. A -c, Ostracoda. A, Falites, a small growth stage, probably just hatched ( x 180) . (From Muller 1979 . ) B, Hesslandona unisulcata. Detail with the naupliar eye on collapsed labrum. Small first and large biramous second antennae ( x 77) . (From Muller 1982 . ) C, Vestrogothia spinata . Preadult stage with six pairs of completely preserved appendages ( x 155) . (From Muller 1979 . ) D - G, Agnostus pisiformis . (From Muller & Walossek 1987.) D, Larval stage lb. Hypostome (centre) with proximal parts of antennulae between cephalic and pygidial shields. Left first trunk appendage also evident ( x 77) . E, Pore on a holaspid ( x 1695) . F, Larval stage 2a with the appendages snugly packed between the shields ( x 220) . G, Trunk appendage of meraspid . Note the fusion of proximal podomeres of endo- and exopodites ( x 1 75) . H, Martinssonia elongata stage 4 ( x 77) . (After Muller & Walossek 1986 . ) I, Skara minuta ( x 90) . (After Muller & Walossek 1985 (Reproduced with permission from the Lethaia Foundation. )

colour corresponding to the Colour Alteration Index 4 - 5 (Section 6 . 2 . 5) . This colour can be produced experimentally by heating the rock to about 300°C . Recrystallization has destroyed the texture in the limestone .

Diagenesis

Dissolution of the limestones in weak acetic acid yields two different types of phosphatic fossils . The first consists of the primarily phosphatic hard parts

276

3 Taphonomy

of groups such as conodonts, inarticulate brachio­ pods, phosphatocopine ostracodes, and various problematica. The other type includes secondarily phosphatized fossils or fragments . A thin coating of phosphate may be deposited on the entire surface, in some cases repeatedly . Alternatively, the original chitinous substance may have been replaced by phosphatic matter. Preservation of this kind is gen­ erally rare and, except for certain somewhat more widely distributed phosphatocopine ostracodes, most taxa are restricted to a few samples only. The detail preserved by phosphatization varies con­ siderably within samples, let alone between the various occurrences . The mechanism o f phosphatization has not yet been determined (see also Section 3.8.4) . It is un­ likely that it occurred in the open sea. Many of the 'Orsten' fossils seem to have been phosphatized prior to decay. As even the finest structures have survived, the animals are assumed to have been buried alive or immediately after death. Extensive picking of residues has produced sev­ eral thousand specimens with preserved soft in­ tegument. Ostracodes such as Hesslandona unisulcata (Fig. lE) are represented by more than one thousand specimens . On the other hand, some other arthro­ pods have yielded only hundreds, tens, or even single individuals . In at least some cases, this dif­ ference in preservation potential between the taxa may be attributed to patterns on the cuticle or to variations in original abundance . The extremely fine preservation even of minor details is due to secondary phosphatization of the body wall, which in most (or all?) cases was chitin­ ous . This may explain the restriction of such preser­ vation to arthropods or arthropod-like organisms and to certain worm-like remains, possibly annelids (see also Section 3 . 8 .4) . Other organic matter be­ longing to an unidentified phylum was not phos­ phatized at all. The occurrence of internal soft organs is rare . Most specimens are three-dimensional and show little if any distortion . Others are wrinkled, and were collapsed or inflated before burial. This is perhaps the result of osmotic differences between body liquid and seawater . Flattening or stretching is not evident, and individuals were not compressed significantly after deposition . This enhances the scope for detailed study compared to that afforded by flattened fossils such as those of the Burgess Shale (Section 3 . 1 1 .2) .

Biota Most representatives of the 'Orsten' arthropod as­ sociation appear to have been benthic or epibenthic. Their body and appendages indicate that the ma­ jority were actively swimming. Forms with legs suitable for walking have not been observed . A suitable habitat may have been a flocculent bottom layer with a high content of nutrients and low currents . The various morphotypes developed adaptations to different life strategies . They may have lived at different levels on or within the soft bottom layer. The 'Orsten' arthropods represent a thanatocoenosis (death assemblage) (see also Section 3 . 5) . Some of them may be autochthonous, while others have been introduced . The most widespread soft-bodied fossils are the phosphatocopine ostracodes (Fig. lA-C) . Their ap­ pendage morphology indicates that they were filter feeders . Dala peilertae and Rehbachiella kinnekullensis may have been similar in this respect. The Skaracarida were cephalomaxillipedal sus­ pension feeders . The more than 100 specimens of the two species of Skara (Fig. 11) represent only adult stages . Bredocaris admirabilis was most likely a suspension feeder. The retention of many larval features into the adult stage indicates that both larvae and adults fed largely on the same source . This is corroborated by the common occurrence of larvae and adults in the same samples . The paddle shape of thoracopods indicates a swimming mode of life . The habitat may have been on, or closely above, the flocculent bottom layer. Martinssonia elongata (Fig. lH) was a bottom dweller that stirred up food with its limbs and its pleotelson-like tail . 'Larva C', a rare form with affin­ ities to the Chelicerata, was ectoparasitic. The trilobite Agnostus pisiformis (Fig . ID-G) is represented by growth stages from the first instar up to the first holaspid (Muller & Walossek 1987) . Although their calcareous exoskeletons are often so abundant as to be rock-forming, phosphatized specimens are extremely rare . Agnostus shows characters quite different from the metameric trilobites . The organization o f the Upper Cambrian arthro­ pods as a whole is surprisingly well advanced . Although they are primitive in important respects, many are closely comparable with Recent taxa, even if a direct evolutionary connection is not very likely. In the absence of evidence for the origin of the arthropods in the Precambrian, it is more likely that

3 . 1 1 Fossil-Lagerstiitten the major evolutionary steps were condensed into a time-span of about 80 million years in the Lower and Middle Cambrian . Small arthropods with preserved soft integument, mainly ostracodes, also occur elsewhere . Similar phosphatization has been found in the Lower Cambrian limestone of Comley, U . K . , the Upper Devonian cephalopod limestone in the Carnic Alps, Italy, the Triassic of Spitsbergen, and in the Lower Cretaceous Santana Formation, Brazil . It is likely that further occurrences will be discovered if the techniques used in processing 'Orsten' limestone are more widely applied to such lithologies .

References Muller, K.J. 1979. Phosphatocopine ostracodes with preserved appendages from the Upper Cambrian of Sweden . Lethaia 12, 1 - 27. Muller, K.J. 1982. HessLandona unisulcata sp . novo with phos­ phatized appendages from the Upper Cambrian 'Orsten' of Sweden . In : R.H. Bate, E. Robinson & L . M . Shephard (eds) Fossil and recent ostracods, pp. 276-302 . Ellis Horwood, Chichester. Muller, K.J. 1985 . Exceptional preservation in calcareous nodules . Philosophical Transactions of the Royal Society of London B311, 67- 73. Muller, K.J. & Walossek, D . 1985a. A remarkable arthropod fauna from the Upper Cambrian 'Orsten' of Sweden .

Transactions of the Royal Society of Edinburgh: Earth Sciences 161 - 172. Muller, K.J. & Walossek, D. 1985b. Skaracarida, a new order of Crustacea from the Upper Cambrian of Vastergotland, Sweden . Fossils and Strata, 17, 1 - 65. Muller, K.J. & Walossek, D . 1986 . Martinssonia elongata gen. et sp . n., a crustacean-like euarthropod from the Upper Cambrian 'Orsten' of Sweden. Zoologica Scripta 15, 73-92. Muller, K.J. & Walossek, D . 1987. Morphology, ontogeny and life habit of Agnostus pisiformis from the Upper Cambrian of Sweden . Fossils and Strata 19, 1 - 124. 76,

3 . 11 . 4 Hunsriick Slate J . BERGSTROM

Introduction The Hunsruck Slate (Hunsruckschiefer) occurs mainly in a belt almost 150 km long, south of the River Mosel in West Germany . It is Early Devonian

277

(Early Emsian) in age . Due to synsedimentary tectonism the thickness varies from less than 200 to 3000 m. In the northwest, 'Rhine an' shallow­ water sediments are dominated by brachiopods; in the southeast are 'Bohemian' distal sediments with the 'classic' faunas . Much of the clay and silt filling the troughs was derived from a land area to the northwest. Sedimentary structures and trace fossils indicate a depth of more than 200 m (Seilacher & Hemleben 1966), while the well developed eyes of arthropods and vertebrates indicate that the water was probably not much deeper than this (Sturmer & Bergstrom 1973) . The Hunsruck Slate fossils are pyritized and often preserved as more or less flattened complete indivi­ duals . In addition to mineralized skeletal parts, the pyritization has affected unmineralized skeletons and true soft parts (Fig. lE, C) . The latter include cnidarian polyps, arthropod muscles and intestines, and soft parts of annelids and molluscs . The sedi­ ment has been transformed to a slate as a result of the Variscan Orogeny, but the cleavage is commonly more or less parallel to bedding, so that the fossils are largely unaffected . The Hunsruck Slate is a conservation Lagerstatte resulting from rapid burial (or obrution) (see also Sections 3 . 6, 3 . 1 1 .4) . The dark colour of the rock is partly due to organic carbon, but the sediment is basically a mineral clay and silt deposit .

Sedimentary environment The average sedimentation rate ranged to a maxi­ mum of a couple of millimetres a year . Thus the various well preserved organisms must have been embedded not by normal sedimentation but by very rapid episodic burial . The animals buried in this way were probably alive in many cases; in others they may have been killed by the current transporting the suspended sediment (Sturmer & Bergstrom 1973; Kott & Wuttke 1987) . This explains why many specimens are lying at a high angle to the bedding planes (Fig. lA) . It also explains the strong dominance of benthic organisms in the fauna . A large proportion of the specimens are complete and articulated . It is well known that echinoderms disintegrate within hours of death, and their excel­ lent preservation also indicates rapid burial. Judging from the vertical and lateral distribution of faunas, such events seem to characterize much of the up to 3000 m thick Hunsruck Slate, although fossils are abundant only in the Bundenbach area . Few of the benthic animals seem to have been able to avoid

278

3 Taphonomy

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Fig. 1 A, Radiograph of undescribed somasteroid species from Bundenbach. Part of single arm ripped off from rest of body; note isolated skeletal elements on the lower side . The arm is much shortened due to deposition at an angle to sediment surface; tip of the arm above. Contrast due to pyritization of skeleton, x 0.9. (After Sturmer et a/. 1980 . ) B, Phacops species from Eschenbach . Careful preparation has exposed fine details of pygidial and four thoracic legs of the right side, x 2.9. (Photograph courtesy of S. Stridsberg. ) C, Undescribed annelid worm from Bundenbach . Segmental pattern indicated by strongly pyritized chaetae, x 3 . 5 . (Radiograph courtesy of w. Sturmer; no . 12852, Senckenberg Museum, Frankfurt am Main . )

being caught by the suspension currents . Occasion­ ally the currents appear to have been powerful enough to tear bodies apart (Kott & Wuttke 1987) but these may have been weakened by partial decay. A good example of this is illustrated in Fig. lA, showing a single arm of an undescribed new so­ masteroid echinoderm. Part of the Hunsruck Slate sequence includes quite thin lenses and extensive laminae of silt. These are interpreted as indicating a distal density current or turbidite (Seilacher & Hemleben 1966) . The undersides of the silt laminae show frequent signs of current activity, such as flute casts and tool marks . These features, in combination with trace fossil evidence, indicate sedimentation in basins in the shelf. The more homogeneous shale is devoid of diagnostic sedimentological features .

Diagenesis The fossils are usually strongly compressed because of the fine-grained sediment. However, early pyri­ tization has preserved much relief (Fig. 1B), more than in other argillaceous deposits, such as the Burgess Shale (Section 3 . 1 1 . 2) . Deposition of small organisms, in particular at high angles to bedding, adds to the deformation caused by compaction. Sliding movements also occurred inside decom­ posing carcasses . In the arthropod Cheloniellon, for example, the ventral side has moved in relation to the dorsal, making the discrimination of the seg­ ments difficult (Sturmer & Bergstrom 1978) . Some authors have suggested that the pyrite was formed mainly in those parts of the animals which contained much organically bound sulphur, e . g . in

3 . 1 1 Fossil-Lagerstiitten the shape of conchiolin, keratin, cystin, spongin, etc. (Fig. lA, C) . The microbial production of H2S played an important role (Section 3 . 8 . 3 ) . In many arthropod specimens the limbs are more extensively pyritized where they extend beyond the carapace, than where they are covered by it. This is probably mainly a function of the high surface area : mass ratio of the exposed limbs, which promotes the reduction of sulphates, compared with that of the main part of the body and adjacent structures .

279

Sturmer, W . , Schaarschmidt, F. & Mittrneyer, H-G . 1980. Versteinertes Leben im Rontgenlicht. Kleine Senckenberg­ Reihe No. 1 1 , pp . 80 Verlag Waldemar Kramer, Frankfurt am Main.

3 . 11 . 5 Mazon Creek G . C . B A I RD

Biota In addition to one acritarch and 47 spores, about 400 species of macrofossils are known from the Hunsruck Slate (Mittmeyer in Sturmer et al. 1980) . The fauna is dominated by benthic and nectobenthic species. Thus, echinoderms form the largest group with some 125 species, closely followed by molluscs with around 1 15 species . Of the molluscs, 92 species are gastropods or bivalves and 31 more or less heavily shelled cephalopods. There are 63 listed species of brachiopods, 31 arthropods, 17 ver­ tebrates, 12 cnidarians, six tentaculite-like forms, six conularids, three bryozoans, one ctenophore, and one red alga. All the arthropods belonged to the benthos, and many of the cephalopods could have done so. The vertebrates are species of agnathans and placoderms which were flattened in life . The flattening provides good evidence that they lived on the substrate . In addition, there is a species of lungfish . A few species form exceptions to this benthic association. These are six species of psilo­ phytes, which must have been derived from a nearby land area, and one pelagic species of each of the hydrozoans and ctenophores .

Introduction

References

The Mazon Creek area fossil localities in northeast Illinois yield a diverse biota of Middle Pennsylvanian plants, terrestrial animals, and numerous aquatic taxa including both estuarine marine and non-marine animals . This biota, pre­ served in sideritic concretions, includes the most important assemblage of soft and lightly skel­ etonized invertebrate animals known from the Late Palaeozoic (Nitecki 1979) . Moreover, it also includes one of the most diverse land plant floras known from North America. Over 350 species of plants, 140 species of insects, and over 100 additional non-marine taxa, including bivalves, millepedes, centipedes, scorpions, spiders, eury­ pterids, xiphosurans, branchiopods, ostracodes, shrimp-like crustaceans, fish, and tetrapods com­ prise the non-marine component which is termed the Braidwood Biota (Baird et al. 1985a) . Estuarine marine organisms, comprising the Essex fauna, are similarly diverse and varied; this component in­ cludes medusae, hydrozoans, a siphonophore, chitons, cephalopods with soft parts, diverse poly­ chaetes and crustaceans, a xiphosuran, a holothu­ rian, several agnathan vertebrates, numerous fish species, and various problematical taxa (Fig. 1 ) .

Kott, R. & Wuttke, M. 1987. Untersuchungen zur Morpho­ logie, Palaokologie und Taphonomie von Retifungus rudens Rietschel 1970 aus dem HunsrUckschiefer (Bundesrepub­ lik Deutschland) . Geologisches Jahrbuch Hessen 115, 1 -27. Seilacher, A. & Hemleben, C . 1966 . Beitrage zur Sedimen­ tation und Fossilfiihrung des HunsrUckschiefers . 14. Spurenfauna und Bildungstiefe der HunsrUckshiefer (Unterdevon) . Notizblatt des hessischen Landesamt fUr Bodenforschung 9 4 , 40 -53. Sturmer, W. & Bergstrom, J . 1973 . New discoveries on trilo­ bites by X-rays. Palaontologische Zeitschrift 47, 104 - 141 . Sturmer, W. & Bergstrom, J. 1978 . The arthropod Cheloniellon from the Devonian Hunsruck Shale. Palaontologische Zeitschrift 52, 57- 81 .

Stratigraphy. Concretions containing the Mazon Creek fossils occur in the Francis Creek Shale Member of the Carbondale Formation which was deposited during the Middle Pennsylvanian Westphalian D stage . The Francis Creek Member is underlain by the widespread and commercially im­ portant Colchester (No. 2) Coal Member; strip mining and deep mining of this coal unit account for the numerous spoil dumps which are the usual collecting sources for these fossils . Where the Francis Creek is thin, it is overlain by the Mecca Quarry Member, a thin, fissile, black shale unit which is

280

3 Taphonomy

Fig. 1 Marine animals (Essex fauna) from Mazon Creek area, northeast Illinois . All specimens from a large strip mine 'Pit 1 1 ' near Essex, Illinois . A , Polychaete annelid Fossundecima konecniorum with conspicuous chitinous jaws, x 1 . 25 . B, Phyllocarid crustacean Kellibrooksia macrogaster, x 1 . 4. C, Palaeoniscoid fish Elonichthys peltigerus, which has choked on an acanthodian fish, x 1 .8 . D, Problematic organism Tullimonstrum gregarium (,Tully Monster'), x 0 . 7 . (All specimens courtesy of Northeastern Illinois University, Mazon Creek Paleontology Collection. )

locally famous for the occurrence of well preserved marine vertebrates; this unit is absent where the Francis Creek Shale exceeds 10 m in thickness. The Francis Creek Shale is variable in thickness regionally, and is absent in many parts of Illinois . It reaches a maximum thickness of 25 - 30 m in northeast Illinois; in the Mazon Creek area it is composed of silty mudstone with local development of coarser deposits, particularly in the upper part of the unit. Fossiliferous sideritic concretions are characteristic of the thickest Francis Creek deposits, and they are usually common in its lowermost four metres. Thin (0 - 5 m) Francis Creek deposits west and southwest of the Mazon Creek area are com­ posed of grey, argillaceous, and distinctly bio­ turbated mudstone deposits which typically lack sideritic concretions (Baird et al. 1986) .

Localities. More than 100 collecting localities for Mazon Creek fossils exist within the Mazon Creek

area, which includes parts of Grundy, Will, Kankakee, Essex, and LaSalle counties . Natural out­ crops of the fossiliferous strata are almost completely restricted to Mazon Creek itself near Morris, Grundy County . Virtually all remaining localities are spoil dumps of abandoned strip mines and underground mines exploiting the Colchester Coal . Most fossil collecting is done in strip mine areas, most notably in one large mine area ('Pit 1 1') near Essex, Illinois . Concretions are continually exposed as the back­ piled tip heaps weather and erode; many of these nodules break open along the fossil plane by re­ peated frost wedging, but others must be split with a hammer.

Sedimentary environment The Francis Creek Shale Member In the Francis Creek area is believed to be an estuarine-deltaic deposit recording the progradational advance of

281

3 . 1 1 Fossil-Lagerstiitten one or more major distributary systems into a shal­ low epeiric sea (Baird et al. 1985a) . The presence of numerous thick, distributary channel sandstones with associated crevasse splay and interdistri­ butary bay deposits indicates that an active coastal delta-distributary complex was present. Braidwood aquatic animals inhabited interdistributary bays and waterways bordering this delta complex. The stratigraphic occurrence of Essex animals in the basal Francis Creek across much of the Mazon Creek area indicates that the delta prograded into a large marine water area . However, the diminutive character of most Essex taxa, the total absence of normal marine shelf organisms (such as corals, bryozoans, articulate brachiopods, trilobites, and crinoids), plus the character of the associated de­ posits, collectively indicate that Essex organisms inhabited a large river-influenced estuary (Baird et al . 1986) . Examination of mud stone deposits associated with these organisms reveals the presence of distinctive cyclic repetitions of mud­ stone and silts tone laminae which appear to record sequential flood- and ebb-tide events within the estuary (Baird et al . 1985a) . Detailed census collecting at all Mazon Creek area localities shows that an abrupt boundary separates areas yielding abundant Essex animals from regions yielding no Essex taxa (Baird et al . 1985a); non­ marine localities near the northeast margin of the census area are abruptly bounded by marine localities to the southwest. However, one-way mixing of plants and non-marine Braidwood animals into areas of Essex animal abundance does occur; this is believed to reflect southwestward (seaward) transport of non-marine taxa by currents from upstream sources (Baird et al . 1985a) .

Diagenesis Mazon Creek aquatic animals generally died as a result of episodic incursions of turbid freshwater during periods of flooding (Baird et al. 1986) . Rapid sedimentation is indicated by engulfment of upright trees, the edgewise burial of plant leaves, and by occasional evidence of escape attempts by bivalves and other organisms (Fig . 2) . The rarity of large animal specimens partly reflects a near-absence of large taxa and/or the successful escape of large animals, but it is also a result of the limited avail­ ability of interstitial iron and organic nutrients re­ quired to produce concretions of sufficient size to enclose large organisms . Mazon Creek fossils are preserved as variably

·.� c�",,,:,o,,. � •.

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Burial of Mazon Creek organisms . Flood event with torrential sedimentation and incursion of freshwater. Organisms include : A, up-ended pinna of Pecopteris; B, partially engulfed medusoid Essexella asherae; C, bivalve Edmondia attempting to escape smothering. (From Baird et al. Fig. 2

1986. )

compressed moulds within concretions . Plant fossils occur as moulds infilled by calcite, kaolinite, or sphalerite with a residue of coaly organic material often present (Baird et al . 1986) . Mollusc shells, cephalopod and chiton radulas, and holothurian pharyngial rings are also preserved as moulds . Medusae are typically composite moulds which re­ flect compressive superposition of top surface detail onto the lower surface following burial; convex­ downward relief on such impressions reflects weight pressing (loading) of the jellyfish lower sur­ face into subjacent muds (Fig. 2) . Most arthropods and some worms retain thin surficial films of variably degraded organic cuticle . Sideritic concretions enclosing fossils serve as a taphonomic 'window' through which important biological information can be obtained because synjacent mud stone deposits yield few well pre­ served fossils . These concretions formed very early following fossil burial; they contain up to 80% carbonate, indicating that they formed in water-rich surface muds (Woodland & Stenstrom in Nitecki 1979) . Most Francis Creek concretions are believed to have nucleated around buried organisms prior to significant decay, and the growth of some may have been triggered or enhanced by decay processes (Fig. 3; see also Section 3 . 8 . 2) . Precipitation of the siderite is believed to have commenced following depletion of interstitial sea water sulphate by sulphur-reducing bacteria; once it was exhausted, bacterial methanogenesis would have commenced, leading to siderite precipitation (Woodland & Stenstrom in Nitecki 1979) . Rapid sedimentation, a weak or unsteady sulphate supply within the estu­ ary, and the entrapment of iron and abundant

282

3 Taphonomy References

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Fig. 3 Early diagenetic events. A, Burial of organism . B, Bacterial sulphate reduction proceeds in local decay centre ('gas vent' zone) above organism prior to depletion of interstitial sulphate . Subsequent bacterial activity produces siderite. C, Continued siderite precipitation hardens proto­ concretion which resists compaction . D, De-watering of surrounding muds causes laminae to deform around nodule . Syneresis (de-watering) within concretion produces fractures which break preformed pyrite (or iron monosulphide) halo around decay centre . (From Baird et al. 1986. )

organic material, are believed t o explain the abun­ dance of sideritic concretions in this deposit (Baird et al. 1986) . A regional preservation gradient is observed within the area of Essex animal occurrence; preser­ vation quality of jellyfish, shrimp, worms, and holothurians decreases to the south and west of Grundy, Will, and Essex counties . In eastern LaSaUe County jellyfish occur as diffuse and often micro­ burrowed impressions, and holothurian remains are sometimes identifiable only from the presence of the coherent pharyngial ring. In western LaSalle County body fossils are rare and the mudstone is highly bioturbated; slower sedimentation near the seaward margin of the delta complex, combined with extensive bottom churning by infauna, account for this poor preservation. Study of similar but younger deposits in Illinois shows that trace-fossil diversity increases seaward of deposits yielding Essex animals, but that body fossils are uncommon between regions of sideritic concretion abundance and normal marine, shell-rich sediments deposited far from shore (Baird et al. 1985b; Baird et al. 1986) .

Baird, G . c . , Shabica, C.W., Anderson, J . L . & Richardson, E . S . , Jr. 1985a. Biota of a Pennsylvanian muddy coast: habitats within the Mazonian Delta Complex, northeast Illinois. Journal of Paleontology 59, 253 - 281 . Baird, G . c . , Sroka, S . D . , Shabica, C.W. & Beard, T . L . 1985b . Mazon Creek-type fossil assemblages in the U . s . midcon­ tinent Pennsylvanian: their recurrent character and palaeoenvironmental significance . Philosophical Transactions of the Royal Society of London B311, 87-99 . Baird, G . c . , Sroka. S . D . , Shabica, C . W . & Kuecher, G . J . 1986. Taphonomy of Middle Pennsylvanian Mazon Creek area fossil localities, northeast Illinois : significance of excep­ tional fossil preservation in syngenetic concretions. Palaios 1, 271 - 285 . Nitecki, M . H . 1979 . Mazon creek fossils . Academic Press, New York.

3 . 1 1 . 6 Holzmaden R . WILD

Introduction The small village of Holzmaden is situated on the northwestern fringe of the Schwabische Alb, about 30 km southeast of Stuttgart in Baden-Wiirttem­ berg, West Germany. It lies in an area of Liassic sediments, of which the Lower Toarcian Posi­ donienschiefer (Fig. 1) contains an abundant, ex­ cellently and completely preserved fossil flora and fauna. Fossils have been known since the end of the sixteenth century, at first from Boll, later from the neighbouring Holzmaden region. In this area, which is protected, some quarries still work and fossils are discovered up to this day .

Sedimentary environment and diagenesis The Posidonienschiefer at Holzmaden consists of 6 - 8 m of thick black bituminous marls and shaly marls with intercalated bituminous allochthonous limestones . The dark colour of the marls is caused partly by diffusely distributed pyrite and partly by organic material. In some layers the latter exceeds 10%, indicating that stagnant conditions persisted for a long period of geological time . The limestones, calcareous nodules and concretions, however, rep­ resent rapid deposition, as shown by obliquely or even vertically embedded uncompressed fossils.

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Stratigraphy of the Posidonienschiefer and distribution of the stratigraphically important ammonites in the quarry G. Fischer, Holzmaden. (After Urlichs et al. 1979 . ) Fig. 1

283

pressed, broken and flattened, except where they are preserved in calcareous nodules, which originate from the decaying organic material. These layers are often enriched by pyrite (see also Sections 3 . 8 . 2, 3 . 8 .3) . Bioturbation horizons (E I 3, E l 4, top of E Ill), consisting mainly of the trace fossil Chondrites, in­ dicate that temporary periods conducive to epiben­ thic life interrupted the otherwise predominantly euxinic conditions . In some beds aligned and mainly juvenile ammonites, or oriented belemnite rostra, point to weak bottom currents . These are also evi­ denced by the disarticulation of vertebrate skel­ etons, or those parts of them, which projected above the embedding mud surface . Benthic organisms are extremely rare in the Posidonienschiefer. They are restricted to some diademoid echinoids, ophiuroids, a few burrowing bivalves (such as Solemya, Goniomya, Cucculaea), and possibly the crustacean Proeryon . The reduced benthic life, the proportionally high percentage of bitumen, the undisturbed sedimentation and the preservation of soft tissues, led to the proposal of a stagnation depositional model for the Holzmaden Posidonienschiefer, and comparison with the quiet-water conditions of the modem Black Sea. An upper water body rich in oxygen and life was underlain by euxinic near bottom water. Kauffman (1979), however, supported a depositional model of black shale-type, pointing out that anaerobic con­ ditions were restricted to the sediment itself, or to a boundary fluctuating between the sediment and the water directly overlying it. His views were superseded by a modified stagnation model incor­ porating storm events (Seilacher 1982) or currents (Riegraf et al. 1984) .

Biota The marls are laminated over a distance of kilo­ metres, as a result of an alternation of clay minerals and enriched organic material, consisting mostly of coccolithophorids . They were deposited slowly, primarily as low-density, water-enriched muds, which were later compacted to about 0 . 17- 0 . 1 of their original thickness . During this early diagenetic process, the pore-water dissolved the aragonite and also partly the calcite of shells, or destroyed micro­ organic hard tissues, so contributing to the lami­ nation (Einsele & Mosebach 1955) . Compaction also resulted in the condensation of shell fragment layers (E II 3, E ll 12) . The enclosed organisms were com-

In the biotic community the autochthonous flora is represented by coccolithophorids. Gingko, the conifers Pagiophyllum and Widdringtonites, the cycadeans Pterophyllum and Otozamites, and the newly discovered Pachypteris, and the horse-tail Equisetites were washed in from the Vindelician continent situated about 100 km south of Holzmaden. The microfauna, stunted in some layers, consists mainly of radiolarians and foraminiferans . Apart from benthic forms, the bivalves Gervillia, Pseudo­ mytiloides, Oxytoma, Exogyra, Antiquilima and possibly Liostrea were fixed by their byssus to a temporarily hardened mud bottom or to floating

284

Fig. 2

3 Taphonomy

Passaloteuthis paxil/osa. Soft body of a belemnite

(Schwarzjura

E

II 1, Ohmden, near Holzmaden) .

shells of mainly ammonites . The bivalves Stein­ mannia, Meleagrinella and Bositra (the earlier 'Posi­ donia', which gave the Posidonienschiefer its name) were pseudoplanktic. The gastropod Coelodiscus is numerous in concretions and limestones; it fed on the decaying organic remains of vertebrates . The ammonites and their stratigraphic distribution are listed in Fig . 1 and by Riegraf et al. (1984) . Coleoids are represented by vampyromorphids (e . g . Loli­ gosepia, Loliginites, Teudopsis, Phragmoteuthis, and Chitinobelus), and the belemnoids Dactyloteuthis, Youngibelus, Salpingoteuthis, and Passaloteuthis . Soft

body tissues of the last are preserved (Fig. 2) . The crinoids Pentacrinites and Seirocrinus lived in colonies, and are often preserved attached to the remains of floating logs . There is a rich ostracode fauna which, together with the crustaceans Uncina, Proeryon, and Coleia, completes the invertebrate fauna of Holzmaden . Holzmaden is famous for its complete vertebrate skeletons . Sometimes they are preserved with the so-called 'skin' (e . g . in £ 11 3 - 5) . This decayed and transformed soft tissue marks the outline of the body as a black film and is found in the sharks Hybodus and Palaeospinax, the holocephalian Acanthorhina, in ganoids and holosteans, but mainly in the many species and specimens of the ichthyosaur Stenopterygius (Fig. 3), in the marine crocodile Steneosaurus (but not in Pelagosaurus and Platy­ suchus), and in the pterosaurs Dorygnathus and Campylognathoides . The pterosaurs and the saur­ ischian dinosaur Ohmdenosaurus are allochthonous faunal elements . Fishes are represented by the ganoids Lepidotes, Dapedium, Pholidophorus, the sub­ holosteans Ptycholepis, Tetragonolepis, and Saurorhyn­ chus, the rare Chondrosteus and rare coelacanth Trachymetopon, and the teleosts Leptolepis and Euthynotus, all of which lived in the oxygen-rich upper water. Some, however, are believed to have been allochthonous (e . g . Lepidotes, Dapedium, Tetra­ gonolepis). The plesiosaurs Plesiosaurus and Rho­ maleosaurus, the ichthyosaurs Stenopterygius and Leptopterygius, and the long-snouted Eurhinosaurus seem to have been inhabitants of the open sea, while the crocodiles and the sphenodontid Palaeo­ pleurosaurus presumably lived near the coast. The ichthyosaur Stenopterygius is represented by many species and hundreds of specimens, some­ times with stomach and intestine contents (e . g . the hooks of coleoids) . There are preserved females giving birth to young (Fig. 4), or containing up to thirteen embryos, or in association with an aborted foetus . The high percentage of pregnant female ichthyosaurs, and of juveniles, may be due to a 'spawning ground' to which the animals migrated periodically over a long geological time to give birth to their young.

References Einsele, G. & Mosebach, R. 1955 . Zur Petrographie, Fossiler­ haltung und Entstehung der Gesteine des Posidonien­ schiefers im Schwabischen Jura . Neues Jahrbuch for Geoiogie und Paliiontoiogie, Abhandlungen 101, 319 -430 .

285

3 . 1 1 Fossil-Lagerstiitten

Fig. 3 €

Stenopterygius macrophasma. Soft body of an ichthyosaur with remains of three embryos in its body cavity (Schwarzjura

II 4, Holzmaden) .

Fig. 4

Stenopterygius qlladriscissus . Female in the process of giving birth, with the remains of three embryos in its body

cavity (Schwarzjura

€

II 3, BoIl) .

Kauffman, E . G . 1979 . Benthic environments and paleo­ ecology of the Posidonienschiefer (Toarcian) . Neues Jahrbuch fUr Geologie und Paliiontologie, Abhandlungen 157, 1 8 - 36. Riegraf, W . , Werner, G . & Lorcher, F . 1984. Der Posidonien­

3 . 11 . 7 Solnhofen Lithographic Limestones G . VIOHL

schiefer, Biostratigraphie, Fauna und Fazies des siidwest­ deutschen Untertoarciums (Lias E) . Enke, Stuttgart .

Seilacher, A. 1982 . Ammonite shells as habitats in the Posidonia Shales of Holzmaden - floats or benthic islands? Neues Jahrbuch fii r Geologie und Paliiontologie, Monatshefte 1982, 98- 1 14. Urlichs, M., Wild, R. & Ziegler, B . 1 979 . Fossilien aus Holzmaden. Stuttgarter Beitriige zlIr Naturkunde, Serie C 11, 1 - 34 .

Introduction The Solnhofen Lithographic Limestones of the Southern Franconian Alb (Bavaria, West Germany) range over an area of about 70 x 30 km and display some differences in facies and preservation of fossils. The Solnhofen Limestones comprise not more than half an ammonite zone in the lower part of the

286

3 Taphonomy

Lower Tithonian, representing at most 0 . 5 myr. The lithology, best described by the German word 'plattenkalke', is characterized by micritic, even­ layered limestone slabs ('Flinze') (mostly with an internal microbedding) and irregularly intercalated calcareous fine-layered marls ('Faulen') .

Sedimentary environment The Solnhofen Limestones were deposited on a sea floor with strong relief, due to algal - sponge reefs . The limestones vary considerably in thickness (0- 95 m) . The depositional area was backreef in position . It was landlocked to the northwest and separated from the Tethys Ocean by discontinuous coral reefs along its eastern and southern margins . All the evidence found in the Solnhofen Lime­ stones suggests a semiarid climate (Viohl in Hecht et al. 1985) . High evaporation rates and the restric­ tion of water exchange with the open sea caused a high salinity and the development of a density stratification in the lagoonal waters . This resulted in stagnation and a hostile bottom environment. Even in the surface water layers the organic productivity must have been relatively low, as can be inferred from the scarcity of fossils and the low content of bitumen and pyrite in the sediment . Only episodi­ cally was the lagoonal water body completely mixed with waters of the Tethys Ocean. The origin of the sediment is still controversial . Barthel (1978) regarded the marly layers (Faulen) as the normal sediment accumulated over a long period, and the limestone layers (Flinze) as rep­ resenting storm events. In this model, which seems the most probable, carbonate ooze deposited on the seaward margin of the coral reefs was periodically stirred up by storms and pushed into the lagoon as a suspension, where it settled down forming a layer of lime mud . Only the finest fraction was transported as far as the basins of Solnhofen and Eichstatt. Other models explain the limestone layers as a kind of stromatolite built up by cyanobacteria (Keupp 1977) or as the result of coccolithophorid blooms (de Buisonje in Hecht et al. 1985) . There are no indications of strong bottom cur­ rents . Evidence of currents, such as roll marks of ammonite shells (Seilacher et al. 1985), orientation of fossils, and ripple marks (Janicke 1969) are con­ fined to the eastern basins (Painten, Pfalzpaint) or to a few beds in the uppermost Solnhofen Lime­ stones which must be interpreted as turbidites caused by earthquakes . In the area of Solnhofen and Eichstatt settling marks next to the fossils (Mayr

1967), as well as aptychi and fragments of ammonite shells lying convex side down, suggest a very calm environment (see also Section 3 . 4 . 1 ) . Other evidence is the high percentage of articulated vertebrates, echinoderms, arthropods (Fig. 1), and ammonites with aptychi in place . The extraordinarily good preservation, in some instances even of soft parts, also required protection by rapid burial . Swept in during storms, the fossils were buried immediately by suspension fallout, because they settled a little earlier than the micritic particles . This could also explain why most fossils lie parallel to bedding . An exception are the jellyfish found in the quarries of Gungolding- Pfalzpaint, which are embedded within the limestone slabs. Being lighter than other animals, they sank only during deposition of the lime mud . The Solnhofen Limestones yield not only well preserved fossils but also disarticulated skeletal el­ ements . These are due to decay processes occurring while the carcasses were floating in the water. Par­ ticularly long drift times, even after decay of the soft parts, can be inferred for belemnites with attached

A characteristically complete specimen of the decapod Eryon arctiformis . (Scale bar 1 cm. )

Fig. 1

=

3 . 1 1 Fossil-Lagerstiitten oysters . Their soft parts have never been found, only those of their relative Acanthoteuthis. Some necrolytic features may be due to the hypersaline environment. Mayr (1967) described strongly bent teleostean fishes with the tail fin torn off the vertebral column . This phenomenon can best be explained by dehydration in a brine, and consequent contraction of the ligaments tying together the neural arches . The caudal fin adhered firmly to the bottom, obviously to a cyanobacterial mat; it could not follow the movement of the carcase and became detached (Fig. 2) . The dorsally bent neck, a familiar feature of Archaeopteryx (Fig. 3), Pterodactyl us, and Comp­ sognathus, is perhaps better explained by the drift­ ing position in which the carcasses came to rest on the bottom (Rietschel 1976) . Seilacher et al. (1985) attributed the post-mortem contraction of the crayfish Antrimpos, and the coiling of the stemless crinoids Saccocoma and Pterocoma, to the dehydrating effect of hypersaline waters . The wrinkles seen in some specimens of the jellyfish Rhizostomites might also be due to the same cause (de Buisonje in Hecht et al. 1985), especially those indistinctly preserved from the Eichstatt quarry area.

Diagenesis In the Solnhofen Limestones two phases of cemen­ tation and correlated compaction must be sharply distinguished:

Fig. 2 A young Tharsis dubius, strongly bent by dehydration in a hypersaline environment. The vertebral column has become detached from the tail fin, itself firmly adhered to a cyanobacterial mat, x 0 . 65.

287

1 An early cementation of the superficial layer was caused by cyanobacterial mats (Keupp 1977) . These were also responsible for the preservation of traces, and they prevented macrofossils from sinking into the underlying soft and mobile sedi­ ment. Syneresis phenomena on the bedding planes (Janicke 1969), formerly interpreted as mud cracks and rain-drop imprints (Mayr 1967), suggest that superficial cementation was accompanied by an early dehydration. 2 The main cementation and compaction of the sediment occurred only after the collapse of fossils, which are therefore all flattened (see also Section 3 . 7) . Compaction could not have continued indefi­ nitely after collapse, however, because defor­ mational structures of adjacent bedding planes below and above the fossil have been preserved. These deformations were plastic in the case of fish, crayfish, and squids (de Buisonje in Hecht et al. 1985) as well as the body chambers of the ammonites Glochiceras and Aspidoceras . During the collapse of shells of the ammonite Perisphinctes, and of the phragmocones of Glochiceras and Aspidoceras, the sediment was already stiffened and reacted by frac­ turing along microfaults (Seilacher et al. 1976) .

Solnhofen fossils typically lie in a depression in the overlying bed while supported on a pedestal in the underlying bed. Depressions ('collapse calderas' of Seilacher et al. 1976) occur on the adjacent bedding planes above and below. Collapse of the fossil cer­ tainly plays an important role in the formation of

288

3 Taphonomy

Fig. 3 The Eichstatt specimen of Archaeopteryx lithographica showing the characteristic post­ mortem dorsally bent neck, x 0 . 65.

pedestals, but other processes are probably also involved (Janicke 1969; Seilacher et al . 1976) . Aragonite must have dissolved in the upper few metres of sediment, as the deformation of am­ monites in slumped layers shows that they have been reduced to periostracal films (Seilacher et al. 1976) . Soft parts are often preserved, e . g . the intestines of fishes (when filled) or the ink sacs of coleoid cephalopods . The ink, consisting of very stable proteins, may survive diagenesis and, dissolved in water, can still be used for drawing (Barthel 1978) . Muscles transformed into phosphate, probably as a result of bacterial activity (see also Section 3 . 8 .4), are preserved in many fishes, coleoid cephalopods, and annelids . In some instances the wing mem­ branes of pterosaurs are still visible as imprints with a phosphatic lining. The soft parts of ammonites have never been found, though their presence at the time of burial is indicated by the aptychi remaining in the shell . These also p revented the body chamber filling with sediment (Seilacher et al. 1976) .

Biota The more than 600 fossil species preserved in the Solnhofen Limestones represent a number of dif-

ferent environments (open sea, coral reefs, lagoon, terrestrial habitats) . A striking feature is the scarcity of autochthonous benthos . The absence of scavengers is a prerequisite for exceptional preservation. Autochthonous epi­ benthos is almost exclusively represented by for­ aminiferans . These indicate a dilution of the lagoonal bottom waters by the influx of great quan­ tities of normal seawater, but obviously such periods of near normal salinity were too short to allow colonization by macrobenthos. The many macrobenthic forms, such as crustaceans, echino­ derms, ray-like sharks, and others, have been washed in by storms . Most of them died during transport. Only the hardiest, such as the horse­ shoe crab Mesolimulus and the crayfish Mecochirus, were still alive on reaching the bottom and left tracks, at the end of which the dead animal can be found (Fig. 4) . The epiplankton includes oysters (Liostrea) (attached to seaweeds), ammonites, and belemnites . The bulk o f fossils were planktic (stemless crinoid Saccocoma, phyllosoma larvae, jellyfish, coccoliths) or nektic (most fishes, cephalopods) . A proportion of these was also swept in, either from the open sea or from coral reefs . However, as the abundant coprolites and some evidence of predation (crushed ammonite shells, half-eaten fishes without any sign

289

3 . 1 1 Fossil-Lagerstiitten

in a storm during flight and drowning (Rietschel 1976) .

References Barthel, K.W. 1978 . Solnhofen . Ein Blick in die Erdgeschichte. Ott Verlag, Thun. Hecht, K., Ostrom, J.H., Viohl, G . & Wellnhofer, P . (eds) 1985 . The beginnings of birds . Proceedings of the International Archaeopteryx Conference, Eichstiitt 1 984. Freunde des Jura­ Museums, Eichstatt. Janicke, V. 1969 . Untersuchungen iiber den Biotop der Solnhofener Plattenkalke . Mitteilungen der Bayerischen Staatssammlung flir Paliiontologie und historische Geologie 9, 117- 181 . Keupp, H. 1977. UItrafazies und Genese der Solnhofener Plattenkalke (Oberer MaIm, Siidliche Frankenalb). Abhandlungen der Naturhistorischen Gesellschaft NUrnberg 37, 128 pp . Mayr, F.X. 1967. Palaobiologie und Stratinomie der Plattenkalke der Altmiihlalb . Erlanger geologische Abhandlungen 67, 40 pp. Rietschel, S . 1976 . Archaeopteryx Tod und Einbettung. Natur und Museum 106, 280-286. Seilacher A., Andalib, F., Diet!, G . & Gocht, H . 1976 . Preser­ vational history of compressed Jurassic ammonites from southern Germany. Neues ]ahrbuch fUr Geologie und Paliiontologie, Abhandlungen 1 52, 307- 356. Seilacher, A., Rei£, W-E . & Westphal, F . 1985. Sedimen­ tological, ecological and temporal patterns of fossil Lagerstatten. Philosophical Transactions of the Royal Society of London B311, 5 -24. -

The decapod Mecochirus longimanatus with settling mark and trail. It was washed into the hostile environment of the lagoon during a storm, sank down and died after a few steps . Only the counterpart of the fossil can be seen as a pedestal . The fossil itself is embedded in the overlying slab, x 0 . 25. Fig. 4

3 . 11 . 8 Grube Messel J . L . FRANZEN

Introduction of decay) indicate, some of the pelagic organisms must have lived in the lagoon itself, at least for short periods . Finally, the Solnhofen Limestones have yielded a wealth of terrestrial organisms . These were either washed-in during rainy seasons (land-plants and reptiles), blown-in by winds (many insects), or they flew actively into the lagoon (pterosaurs, Archaeopteryx) . The only way in which complete skeletons of Archaeopteryx (Fig. 3) or pterosaurs could have been preserved is by becoming caught

Grube Messel is a former opencast oil shale mine, located about 30 km southeast of Frankfurt, West Germany. The crater left after mining ceased in 1971 is 60 m deep and 700 - 1000 m wide . Its horizontal extent corresponds almost exactly with the occur­ rence of the so-called oil shale, a laminated, dark brown- olive green clays tone with a petroleum content of 5 - 20% . In cross-section the formation is lenticular. Its maximum thickness was originally 190 m. It was covered by as much as 5 m of a black clay and by up to 33 m of multicoloured argillaceous sediments limited to three troughs in the southeast.

290

3 Taphonomy

Underlying the oil shale are up to 25 m of coarse sediments (Weber & Hofmann 1982) . Surrounded by Upper Palaeozoic sediments, diorites, and granodiorites, these Early Tertiary sediments are preserved within a tectonic graben . This was part of a large rift lake system, accompanied by early rift volcanism connected with the incipient formation of the Oberrhein Graben (Matthes 1966) .

Sedimentary environment Judging by its fossil content, the bituminous clay­ stone was originally deposited on the bottom of a small lake at the beginning of the Middle Eocene (Early Lutetian, Early Geiseltalian), about 49 ± 1 Ma. Except for one restricted occurrence in the north, and some debris flows in the south, nearshore sedi­ ments have already been eroded. The lake covered only a few square kilometres and was at least some

tens of metres deep . It was surrounded by a dense rainforest (Thiele-Pfeiffer in Ziegler 1986) . With a mean annual temperature of at least 20°C, Lake Messel must have been of warm-monomictic sub­ tropical type (Franzen et al . 1982) . The Fossil-Lagerstatte is a limnic stagnation de­ posit (Seilacher et al . in Whittington & Conway Morris 1985) . From time to time the lake was con­ nected with a river system and acted like a settling tank (Franzen in Whittington & Conway Morris 1985) . All the preservable parts of organisms drift­ ing downstream, or once living in the lake itself, were ultimately embedded in the argillaceous sedi­ ments of the lake bed . There anoxic conditions pre­ vailed because of the low energy environment, and a high consumption of oxygen resulting from the decomposition of masses of micro-organisms (mainly algae) that flourished under a tropical- sub­ tropical climate . Thus reducing conditions appeared

Fig. 1 Complete articulated skeleton of an Eocene turtle (Trionyx messelianus) from the Grube Messel, x 0.25. (Photograph courtesy of E. Haupt, Senckenberg Museum. )

3 . 1 1 Fossil-Lagerstiitten which prevented the development of any benthic macro-organisms . Therefore there was no bio­ turbation. Vertebrate carcasses were completely buried at the bottom of the lake and were neither destroyed by scavengers nor disturbed by currents . They did not rise again to the surface because the pressure of the water column was sufficiently high to prevent inflation of their bodies by the gener­ ation of decomposition gases. Thus their carcasses were routinely preserved as complete and articu­ lated skeletons (Fig. 1 ) . Reducing conditions near the bottom, o r within the uppermost layers of sediment, led to the forma­ tion of typical minerals such as side rite, marcasite, pyrite, and vivianite (Matthes 1966) . Within certain

Fig. 2 Eocene bat PaZaeochiropteryx tupaiodon from the Grube Messel, displaying its body outline together with the patagium (flying membrane) as a black silhouette, x 1 .4 . The bones within the body were dissolved during diagenesis. (Photograph courtesy of C. Schumacher, Senckenberg Museum. )

291

horizons early diagenetic phosphatic minerals such as messelite and montgomeryite also developed (Schaal in Schaal 1987) . The fine lamination of the clays tone is due to annual climatic fluctuations . It consists of algal-rich layers caused by seasonal blooms which were superimposed on a steady background sedimen­ tation of smectite and other clay minerals (Goth in Ziegler 1986) . The sedimentation rate was low (about 0 . 1 mm per year) . It was occasionally inter­ rupted by slumps coming down the slopes . In any case it can be assumed that the Messel lake existed for hundreds of thousands of years in a lowland area.

292

3 Taphonomy

Biota The fossils comprise plant remains (algae, fungi, diatoms, pollen, leaves, blossoms, fruits, seeds, and fragments of branches), spiculae and even gem­ mulae of freshwater sponges, gastropods, ostra­ codes (moulds only), thousands of insects (mainly Coleoptera, Hymenoptera, and Heteroptera; but also Odonata, Plecoptera, Blattodea, Isoptera, Saltatoria, Phasmatodea, Homoptera, Trichoptera, Lepidoptera, and Diptera), spiders, freshwater shrimps (very rare), freshwater fish (except for one eel), one salamander, frogs, turtles, lizards, snakes, crocodiles, birds, and about 35 species of mammals (Marsupialia, Proteutheria, Lipotyphla, Chiroptera, Primates, Creodonta, Carnivora, Condylarthra, Pholidota, Xenarthra, Perissodactyla, Artiodactyla, and Rodentia) . Lungfishes are only represented by their coprolites . The Messel locality has also gained renown as a treasure trove of little-altered chemo­ fossils (Franzen & Michaelis 1988; see also Section 3 . 2 ) . Biomarkers among these even indicate archaebacteria . Paradoxically, flying animals (insects, birds, and bats) are superabundant, while water-dwelling in­ sects are lacking, except for those transported into the lake . This may be evidence of occasional pol­ lution of the lowermost atmosphere by carbon dioxide, which could also account for the many ground-dwelling vertebrates found in relaxed pos­ itions typical for such a death (although drowning may also produce this posture) (Franzen et al . 1982) . This hypothesis is supported by the fact

that bats which display a wing construction es­ pecially suited for flight close to the ground (Palaeochiropterygidae) are far more abundant than those typically adapted for flight at high speed and considerable height (Hassianycterididae) (Habersetzer & Storch in SchaaI 1987) . Alternatively, water-dwelling insects (as well as fish) could have been affected by oxygen deficiency and/or poison­ ing by hydrogen sulphide and/or ammonia, both generated by the annual turnover of the lake, and/or by tanning agents produced by decompo­ sing plant material (Lutz in Schaal 1987) . The quality of preservation is really exceptional. Plant remains often display not only delicate and soft tissues, but also feature more complete struc­ tures such as fruiting heads (Collinson in Franzen & Michaelis 1988) . Collagen fibrils have been de­ scribed from freshwater sponges. Insects still show colours of their original pattern. Vertebrates, in general, are not only preserved as complete skel­ etons, but also display various stages of ontogenetic development (including pregnant early horses with embryos; Franzen in Ziegler 1986) . On occasion, vertebrate skeletons are surrounded by a black shadow tracing the former outline of the soft tissue including the detailed structure of feathers, or the tips of the hairs (Fig. 2) . Nevertheless the soft parts of the vertebrates are not directly preserved, only their silhouettes (Wuttke 1983) . Scanning electron microscope studies revealed minute bodies in the form of rods or grains of siderite (see also Section 3.8.2). Evidently these originated from a dense covering of bacteria, which

Fig. 3 Bacteria (autolithified as siderite) preserving the fur of an Eocene primate (Europolemur koenigswaldi) as a black shadow. Scanning electron micrograph, x 4250. (Courtesy of G. Richter, Senckenberg Museum . )

3 . 1 1 Fossil-Lagerstiitten

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293

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i n f i l t rat i o n of bact e r i a l ayers a u to l i t h i ficat i o n of decompos i n g t--� bacte r i a as s i d e r i te ( FeC0 3 ) Fig. 4 Factors involved in the exceptional preservation o f articulated skeletons, and so-called soft parts o f Eocene vertebrates and insects from the Grube Messel (West Germany) . (After Franzen in Whittington and Conway Morris 1985 . )

had begun to decay the carcasses as soon as they were deposited on the lake bed (Fig. 3) . Apparently, the bacteria then became petrified through their own metabolic production of carbon dioxide and the precipitation of iron which was present in the lake as a result of the weathering of igneous rocks and Permian red beds nearby. Only later did this thin 'lawn' of autolithified bacteria become a black silhouette, through infiltration and cementation by further organic material derived from plants . In this way, the soft part contours of the Eocene ver­ tebrates have been handed to us not directly, but by a natural replication which could be called 'bacteriography' . Genuine preservation of soft tissue, like cell walls of plants, hairs of mammals, or scales from the wings of moths, sometimes occurs within gut con­ tents . They reveal remnants of the diets of om­ nivorous, insectivorous, carnivorous, folivorous, frugivorous, and even fungivorous mammals (Richter in Schaal 1987) . Occasionally, even fish, snakes, and insects (pollen; Schaarschmidt in Ziegler 1986) preserve digestive remains. Although the whole taphonomic context is still far from completely understood, a generalized dia­ gram of the factors involved in the extraordinary

quality of the preservation of fossils at Messel can be presented (Fig. 4) .

References Franzen, J.L. & Michaelis, W. (eds) 1988. Der eozane Messelsee. Eocene Lake Messel . Courier Forschungsinstitut Senckenberg 107, 1 -452 . Franzen, J . L . , Weber, J. & Wuttke, M. 1982 . Senckenberg­ Grabungen in der Grube Messel bei Darmstadt. 3 . Ergebnisse 1979 - 1981 . Courier Forschungsinstitut Senckenberg 54, 1 - 1 18 . Matthes, G . 1966 . Zur Geologie d e s Olschiefervorkommens von Messel bei Darmstadt. Abhandlungen des Hessischen Landesamtes fiir Bodenforschung 51, 1 - 87. Schaal, S . (ed . ) 1987. Forschungsergebnisse zu Grabungen in der Grube Messel bei Darmstadt. Courier Forschungsinstitut Senckenberg 91, 1 - 2 1 3 . Weber, J . & Hofmann, U . 1982. Kernbohrungen in der eozanen Fossillagerstatte Grube Messel bei Darmstadt. Geologische Abhandlungen Hessen 83, 1 - 58. Whittington, H . B . & Conway Morris, S . (eds) 1985 . Extra­ ordinary fossil biotas: their geological and evolutionary significance . Philosophical Transactions of the Royal Society of London B311, 1 - 192 . Wuttke, M. 1983 . 'Weichteil-Erhaltung' durch lithifizierte Mikroorganismen bei mittel-eozanen Vertebraten aus den Olschiefern der 'Grube Messel' bei Darmstadt. Senckenbergiana lethaea 64, 509 -527.

294

3 Taphonomy

Ziegler, w. (ed . ) 1986 . Wissenschaftlicher Jahresbericht 1985 des Forschungsinstituts Senckenberg, Frankfurt am Main . Courier Forschungsinstitut Senckenberg 85, 1 - 348.

3 . 1 1 . 9 Baltic Amber T . S C H LUTER

Introduction Fossil resins embedded in any type of sediment are normally called 'amber' or, in the case of stratigra­ phically younger examples 'copal' . Unquestionably Baltic amber is the world's most famous . Its name is derived from the fact that it is abundant along the shores of the Baltic sea, especially in the vicinity of the Samland Promontory in the U . 5 . 5 . R . Baltic amber has been known since neolithic times and recognized as a derivative of trees since antiquity, when Aristotle, Pliny, and Tacitus de­ scribed some of its physical, chemical, and biological properties . However, from medieval times up to the eighteenth century, knowledge of its origin was almost lost. Baltic amber has been commercially exploited for centuries by beach collecting, dredging, and mining. Important amber trade routes from the Samland carried raw and polished amber (the 'gold of the north') into the Mediterranean region, where amber is known from many archaeological sites . Later, most Baltic amber was used in high grade varnishes. Today, the bulk is used for making jewellery.

Autochthonous and allochthonous amber Lagerstatten A model for the formation of autochthonous and allochthonous amber Lagerstatten was presented by Dietrich (1979) . Generally Baltic amber now occurs only in secondary or allochthonous deposits, but originally an autochthonous preservation and con­ centration of this fossil resin is likely, as evidenced by the depositional environment of Recent and subfossil copal . The resin sometimes accumulates in the soil around the tree from which it falls, aided by its relatively high resistance to chemical, physical, and biological degradation. Under anaerobic or reducing conditions, resin is concentrated during the formation of peat (especially in subtropical and tropical climates), and concentration might increase during the formation of coal. The main factor in resin concentration under aerobic or oxidizing conditions is the decompo­ sition of the other non-bituminous substances . The likelihood of preservation of such layers increases when the resin, once concentrated, is then protected from decomposition by the onset of anaerobic conditions. Whilst autochthonous deposits of resins are gen­ erally restricted to coal-bearing deposits, al­ lochthonous deposits have been formed in various environments where transport mechanisms played

Sedimentary environment Baltic amber is derived largely from the extinct tree Pinus succinifera (gymnospermid family Pinaceae), which flourished during Early Tertiary times (50 35 Ma) on a land mass that reached southward to the vicinity of the Samland (Fig. 1 ) . This area became inundated in the Late Eocene or Early Oligocene and the resin left behind by the forests that grew there was washed out by the sea and/or ancient rivers . Today it is associated with an originally marine sediment called 'blue earth', from which it is continuously eroded, partly transported and sometimes redeposited at some distance (Fig. 1 ) .

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3 . 1 1 Fossil-Lagerstiitten an important role . In allochthonous deposits the formation of amber Lagerstatten depends largely on the hydrodynamic qualities of each amber particle, which in turn depends on the density, size, and shape of the respective amber variety . Being scarcely heavier (sometimes even lighter) than water, re­ worked amber can be carried in suspension even in conditions of little movement. Concentrations of amber are thus deposited where water movements slacken . The maximum diameter of amber particles which can be transported increases with water den­ sity (as a result of higher salt content) . The largest Baltic amber particles have a weight of approximately 10 kg (Andree 1951). The following amber Lagerstatten can be distinguished: continental basins (including terminal lakes), areas subjected to fluvial flooding and deltas/estuaries, limnic and marine drift lines, tranquil bays, and submarine depressions (Fig. 2) . The richest Baltic amber-bearing deposit is the bed of the upper blue earth in the Samland, which consists of glauconitic sands containing typical marine fossils. Here the index fossil Ostrea venti­ labrum, indicating a lower Oligocene age, is very common. Approximately 15 m below lies the lower blue earth, which is comparatively poor in amber and assigned to the Upper Eocene .

Fig. 2

295

Baltic amber as a trap Generally in both Gymnospermae and Angio­ spermae, resin is produced by parenchyma cells that usually line rounded pockets or cysts, and elongated canals (Langenheim 1969) . Two different possibilities for the development of these cell types exist: (1) the schizogenic mode involves the separ­ ation of cells which round off and increase their intercellular spaces to produce pockets or canals of which the secretory cells form an epithelial layer; and (2) the lysigenic mode results in the formation of cavities from the breakdown or disintegration of the secretory cells . Often the process of production of resin is a combinaton of both types . In practice resin often flows from cracks which develop as a result of tension or wounds in the bark. The resin is then exuded on trunks and branches in amounts depending on the productivity of the particular species . The so-called 'schlauben', and the drops of amber, are the typical preservation mode (Fig. 3) . Schlauben arose as a result of a number of resin flows at brief intervals . Resin warmed by the sun flowed in a relatively fluid form down the tree trunk, followed by inhibition of the flow by cooling during the night, when the surface partly solidified .

Possible autochthonous and allochthonous deposits o f amber.

296

3 Taphonomy

Fig. 3 The formation of resin . The schlauben are most effective as potential traps. (After Katinas 1971 . )

However, large quantities of resin are also stored inside the tree's trunk, in major lysigenous fissures in the wood and the bark. Such places do not act as potential traps for the tree's inhabitants and visitors . Resin of this type is normally empty of animal inclusions, and is represented in the Baltic amber by the so-called 'fliesen' and plates. The fossilization potential of resin exuded and exposed is quite variable . Hence the animal in­ clusions of the Baltic amber represent members of several different niches in the original forests . Larsson (1978) noted that the amber tree was in­ habited by a series of different animal species, only a few of which were specific, mainly phytophagous, while others were indifferent to the identity of their host plant, or were random guests . Inhabitants of the following niches were differentiated: plant­ sucking insects, leaf- and seed-consumers, gall producers, nectar seekers, insects and spiders trapped while resting, the fauna of moss and bark, and the hidden fauna of tree trunks .

Biota Then fresh resin flowed over that of the previous day. The earlier formed resin skin was a most effec­ tive trap for capturing arthropods (which often struggled to free themselves, as may be seen from the whirls created in the amber by legs, wings, etc . ) . Subsequent flows sealed their transparent tomb (Larsson 1978) .

Generally the fauna of the Baltic amber is dominated by Diptera (Fig. 4) (approximately 50% of all animal inclusions and represented by both Nematocera and Brachycera), whilst in other fossiliferous resins - especially those formed under tropical conditions - Hymenoptera and Diptera account for almost equal percentages (Fig . 5) (Schhiter 1978) .

Fig. 4 A species of Diptera: Empididae from the Baltic amber.

3 . 1 1 Fossil-Lagerstiitten

297

50% 40% 30% 20% 1 0% 2

3

4

Fig. 5 Relative frequency of different higher systematic groups of animals in Baltic amber (anterior darker columns) and in amber of the Dominican Republic (Oligocene) (posterior lighter columns) .

In Baltic amber the percentage of Hymenoptera (only 5%) is exceeded by that of Apterygota (1 1%), Acarina (9%), Rhynchota (7%), and Trichoptera (6%) . Coleoptera and Araneae account for approxi­ mately 5% each, and all the other higher systematic groups together for less than 2% (including myria­ pods, snails, and the very rare hairs of mammals, feathers of birds, and at least one almost complete lizard) . Fossiliferous amber-bearing deposits range stratigraphically down to the Lower Cretaceous, although fossil resins are recorded as early as the Carboniferous . Baltic amber has provided by far the most inclusions . However, a higher frequency of fossils per quantity of resin occurs in tropical regions (e . g . amber of the Dominican Republic, and dif­ ferent types of copal) . Since the inclusions of almost all fossiliferous ambers are extraordinarily well preserved, micro­ scopic details of the specimens can sometimes be enlarged by approximately 1000 times . These fossils are interesting not only in themselves, but also because they provide evidence of the development and dispersal of the taxonomic groups they rep­ resent. Such information is basic to a proper under-

standing of the phylogeny and biogeography of present-day forms, and it allows conclusions to be drawn about the ecological and climatic character­ istics of the area in which they lived.

References Andree, K. 195 1 . Der Bernstein. Das Bernsteinland und sein Leben . Franck'sche Verlagsbuchhandlung, Stuttgart. Dietrich, H-G . 1975 . Zur Entstehung und Erhaltung von Bernstein Lagerstatten - 1: Allgemeine Aspekte . Neues Jahrbuch fUr Geologie und Palaontologie, Abhandlungen 149, 39 - 72. Katinas, V. 1971 . Amber and amber-bearing deposits of the southern Baltic area. Transactions of Lithuanian Scientific Research, Geological Survey 20, 1 - 151 (in Russian) . Langenheim, J.H. 1969. Amber: a botanical inquiry. Science 163, 1 157- 1 169 . Larsson, S . G . 1978. Baltic amber - a palaeobiological study . Entomonograph 1, 1 - 192. Schlee, D . & GlOckner, W. 1978 . Bernstein . Bernsteine und Bernstein - Fossilien . Stuttgarter Beitrage zur Naturkunde CS, 1 - 72 . Schliiter, T. 1978 . Zur Systematik und PaIaokologie harzkonservierter Arthropoda einer Taphozonose aus dem Cenomanium von NW-Frankreich. Berliner Geowissenschaftliche Abhandlungen A9, 1 - 150.

3 . 12 Completeness of the Fossil Record C . R . C . PAUL

the ratio of short-term to long-term sedimentation rates, usually expressed as a percentage . Since me­ dian short-term sedimentation rates vary very widely in different environments, only the rates for the appropriate environments can be used to cal­ culate this ratio . Even so, completeness has been defined as the proportion of intervals of a given duration (e . g . 10 000 years) represented within a measurable thickness of sediment, and this propor­ tion varies with the time interval chosen . The same section may be complete at a resolution of one million years, but very incomplete on a time-scale of millenia or centuries . This follows from the defini­ tion of completeness . When an interval is repre­ sented by a measurable thickness of sediment, it does not mean that the sediment accumulated con­ tinuously throughout that interval (Fig. 1 ) . Thus a 1 million year interval may be represented by 1 m of sediment, all of which was deposited in a thousand years . Under the definition given above, the section

Introduction Completeness may be defined or estimated in sev­ eral ways. The completeness of the sedimentary record limits that of the fossil record (and not all sediments are fossiliferous) . It is usually expressed as the proportion of time actually represented by sediments . Equally, completeness of the fossil record may be defined in terms of the proportion of all the species that have ever lived which are known as fossils, or in terms of how accurately we know relative abundances, geographical or stratigraphic ranges, etc. In short, degree of completeness is relative to some predetermined objective, which also defines the type of information required . To construct a faunal list requires a single identifiable fragment of a fossil; to describe that fossil requires a complete, well preserved individual; to establish its relative abundance requires a large sample of fossils, whereas to determine its geographical or strati­ graphic range requires samples from many localities and horizons . Thus the same data may be complete for one purpose, but incomplete for another. The related, but separate, concept of adequacy is also defined by the initial objectives, and the complete­ ness of the fossil record may be quite irrelevant to its adequacy . Too often incompleteness has been equated with inadequacy. If that were true gener­ ally, all science would be inadequate since no science is based on complete knowledge .

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Completeness of the sedimentary record Here the objective is to estimate in a given section the proportion of time actually represented by sedi­ ment, and it has often been asserted that bedding planes represent more time than the beds they bound . Estimates are made by determining median short-term sedimentation rates in different modern environments, using a very large sample of pub­ lished values, and then comparing them with median long-term sedimentation rates for that par­ ticular section (e . g . Retallack 1984) . Long-term sedimentation rates are calculated from observed thickness and estimates of total duration taken from published radiometric time-scales . Completeness is

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298

3 . 1 2 Completeness of Fossil Record would be complete at a resolution of 1 million years, but only 0 . 1 % complete at a resolution of millenia since 999 of the 1000-year intervals would not be represented by any measurable thickness of sediment. Estimates of completeness of a wide range of sedimentary successions determined by this method are very low at a resolution of 1000 or even 10 000 years (Schindel 1982), and it was originally concluded that most sedimentary successions are far too incomplete to determine, for example, whether speciation events were gradual or punc­ tuational (Schindel 1980) . However, there is a flaw in the calculation of short-term rates of sedimen­ tation which tends to maximize them. Where thickness of accumulated sediment is too small to measure (including all zero values), no one in fact records this . Thus published values of short term sedimentation rates are biased and, furthermore, the greater the variance of the sedimentation rates, the greater the effect of this bias on calculated median short-term rates. Anders et al. (1987) pres­ ented a method of overcoming this bias. For pelagic sediments they suggested that short-term and long­ term sedimentation rates are almost identical and therefore that many pelagic sections are nearly complete . Even in other environments where the sedimen­ tary record is genuinely more incomplete, different sections are unlikely to have precisely the same time intervals represented by sediment or by gaps. Thus analysis of the time intervals actually rep­ resented by sediment, combined with improved quantitative methods of correlation between sec­ tions, offers the possibility of more refined strati­ graphy and improved levels of resolution of palaeontological events.

Completeness of the ultimate fossil list In this case the aim is to estimate the proportion of all species that have ever existed which are known as fossils . Consequently only the presence/absence of data is under consideration. To test this we need a situation where it is known that an organism ex­ isted but has not been found . Gaps in the strati­ graphic record of fossils provide just such a situa­ tion. A gap occurs where a fossil is known from below and above, but not actually within, a given horizon . Such fossils have been called 'Lazarus taxa' . Provided any Lazarus taxon is correctly identified at its known horizons, it must have existed during any intervals between them. Thus, analysis of gaps

299

provides a crude quantitative estimate of complete­ ness, but again precise values depend on both the taxonomic and strati graphic levels of the analysis . Analysis of gaps provides a minimum estimate of incompleteness because gaps may exist beyond the known ranges of Lazarus taxa, in addition to the detectable ones between their first and last known occurrences . Equally, fossils found in a single strati­ graphic interval cannot have gaps in their ranges and are best omitted from such analyses. A cladistic or phylogenetic analysis of taxa can detect gaps beyond known ranges, but only for those taxa that left descendants . There is always the possibility that real ranges extended beyond the apparent point of extinction of a clade . Despite this drawback, analysis of gaps is very instructive in providing estimates of completeness . Fig. 2 represents data for 18 cystoid families at series- stage level to illustrate the principles of the method . Total range is 107 stratigraphic intervals, total gaps 26; hence the cys­ toid fossil record is at least 25% incomplete at the family- series level of analysis . Analysis of gaps at the ultimate level of species in samples provides the highest values for incompleteness . Even here, values are around 40% for Cretaceous ostracodes, implying that as much as 60% of the record might be known. Analysis of gaps has additional spin-offs . The largest gap so far encountered in the echinoderm fossil record proved to be an artifact of taxonomic misinterpretation . The edrioasteroid family Cya­ thocystidae used to contain two Lower Ordovician and two Middle - Upper Devonian genera with nothing known between . Redescription of the Ordovician genera showed them to be morpho­ logically unique and not at all closely related to the Devonian forms . Hence this large gap disappeared. Analysis of gaps directs attention to such taxonomic errors . Equally, cystoids have an exceptionally poor fossil record in the Llandovery . Whatever the reason for this, it inevitably accentuates the apparent major extinction of cystoids at the end of the Ordovician. Of 14 Upper Ordovician cystoid families, eight are known to have survived into the Lower Silurian but only one is actually represented by fossils in the Llandovery. The exceptionally poor fossil record of cystoids in the Lower Silurian casts doubt on whether all the other six families really did become extinct at the end of the Ordovician. Again analysis of gaps directs attention to stratigraphic anomalies . Growth of knowledge of the fossil record is also a crude estimator of completeness . If only a small proportion of all organisms is known, then new fossiliferous localities would yield fossils most

3 Taphonomy

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of which would be new to science . Alternatively, if we already knew most of the organisms that ever existed, discovering new ones would become a rela­ tively and increasingly rare event. This type of analysis cannot be done simply by examining the rate at which new taxa are being described . Many new taxa, particularly those above specific rank, simply result from taxonomic refinement. If two formerly congeneric species are reassigned to two separate genera, one genus may be new but still based on a species first described last century, and the total number of species known has not increased at all . The way around this problem is to assign all taxa in the sample to one classification, preferably the most recent or thorough, and then to determine when the first representative of each constituent taxon was originally described (irrespective of the taxon to which it was assigned at the time) . For example, when the first two species of cystoids were described in 1772 they were thought to be

Fig. 2 Ranges of cystoid families known from more than one series, to show gaps (G) as well as total range (T) . Known occurrences indicated by solid lines, gaps by dots . Rows give proportion of gaps for each family; columns for each stratigraphic interval. In both cases Grr yields the proportion of gaps . (After Paul 1982.)

related to the modern sea urchin Echinus . They are now placed in separate classes, and Echinus in a third. Nevertheless those cystoids represent the first examples of the two classes ever described, even if the classes themselves were not recognized un­ til much later . Using such techniques curves de­ scribing the rate at which genuinely new taxa have been discovered can be drawn up (Fig. 3B) . These curves show that for cystoid families the pace of discovery has slowed (only three new families since 1900 and one of those based on specimens dis­ covered last century but left undescribed for over 75 years) . The numbers of genuinely new genera and species have risen significantly since 1900, by over 50%, and 100%, respectively. These curves imply that the majority of cystoid families are already known, but there are probably many more genera and certainly more species to be discovered. Hence rare fossils may be rare not because the fossil record is incomplete, but because they were originally

301

3 . 1 2 Completeness of Fossil Record A

.£ a;

1 00 5

V>

.2: -0
C


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fauna), then when a fossil from sample L + 1 is identified the probability (p) that it will be species x is 0 .01 (or 1%), and the probability that it will be something else (q) is 0 . 99 (or 99% ) . (p + q 1 because there are only two possible outcomes.) As more fossils are identified the total probability (Q) of species x being overlooked declines as follows :

50

=

0

B

Time �

1 00

50

o �����--.----,---.--� 1 775

1 800

1 850

1 900

1 950

2000

Fig. 3 A, Theoretical growth of knowledge curve . The longer fossils are collected, the greater the proportion of total diversity that will be discovered. Average slopes from 1900 to date (Fig . 3B) suggest that the proportion of cystoid families (F), genera (G), and species (5) already known are as indicated. B, Actual plots of the growth of knowledge of cystoid taxa to date . All three curves normalized to present day diversity (shown in parentheses). (After Paul 1982.)

rare animals . Analysis of gaps for several major echinoderm groups showed that the rarest forms, the cyclocystoids, had the most complete record, whereas the blastoids (the most diverse group treated by the analysis) had the most incomplete record.

Completeness of stratigraphic ranges Here the objective is to estimate how accurately the stratigraphic range of a fossil is known . (The argu­ ments may be applied to other relative information from the fossil record such as geographical range or specific abundance .) Shaw ( 1964) approached the problem from the point of view of sample size . In a section fossil x is present up to sample L, but absent in the next sample (L + 1 ) . Shaw asked how one could test whether fossil x was in fact present, but had been overlooked . He argued that in any sample all taxa fall into two groups; they are either species x or they are something else. If we suppose that species x is present but rare (say 1% of the preserved

Q

=

qn

=

(1

_

p) n ,

where n number of fossils identified . Thus sample size and the proportion of the total fauna that a given taxon constitutes (i. e . n and p) determine the probability of overlooking that par­ ticular fossil . Hay (1972) published an extensive graph of values for n, p, and Q. Note that we can never be certain that a species has not been over­ looked. As long as one fossil remains in the rock it might be a specimen of the species sought. However, sample size does enable us to estimate the chances that we have overlooked a fossil and hence not determined its range accurately . It follows that the required sample size should be determined by the degree of confidence with which stratigraphic ranges need to be established . Furthermore, bulk sampling is more likely to detect all species present, than picking from exposed surfaces . Where the latter is unavoidable, stereological techniques should be used to assess relative abundances (McKinney 1986) . The chances of a random section, such as a quarry face, cutting through a fossil not only depend on its abundance but on the size and shape of the fossil as well . Small species are less likely to be encountered than large ones, whereas spherical fossils are more likely to be cut than disc- or rod-shaped ones. Paul (1982) approached the problem from a dif­ ferent standpoint. To determine any range requires at least two specimens from different horizons . A range based on just two fossils is unlikely to be even approximately complete, whereas one based on a very large number of examples is unlikely to be significantly incomplete, unless some special cir­ cumstances prevail. Paul argued that if, throughout a section, the chances of a specimen being preserved were equal and the sedimentation rate was more or less uniform, then the frequency distribution of intervals between specimens of the same taxon should follow an exponentially declining curve identical to the radiometric decay curve . In this case the median interval would be an estimate of the 'half interval' (i, equivalent to the half-life of radio­ metric decay) and could be used to put confidence intervals on known ranges (Fig. 4) . Thus 95 and =

3 Taphonomy

302 m

2

20

15

10

l

>­ u c Q) � u

�

Reliability of sequence S p ec i m e n s

u..

5

o

I nt e rva l

Fig. 4 Derivation of frequency curves from intervals in a measured section . The actual occurrences of specimens are plotted in column 1 . The intervals between them are shaded according to size (column 2), in classes that are multiples of the median interval (i) . The frequency histogram is derived from these intervals . Confidence limits (95%) are ±4i above and below known range . (After Paul 1982 . )

99% confidence intervals are approximately ±4i and ± 7i, respectively (the exact figures are 93 .75 and 99.22%). Comparisons o f real distributions with the ideal curve showed that some did satisfy the initial as­ sumptions . In other cases it is usually possible to determine which of the two assumptions is invalid, because significant changes in sedimentation rate should affect all fossils which range through that part of the section. One case was particularly in­ structive . The trilobite Grandagnostus falanensis had a single enormous gap in its range . The brachiopod Lingulella showed the expected frequency distri­ bution throughout the section, implying that sedi­ mentation rates were uniform. Another agnostid trilobite ranged through the gap, which was there­ fore unlikely to be due to diagenesis destroying G. falanensis, or to this trilobite being overlooked . Paul concluded that G. falanensis was not preserved through this interval because it was originally absent from the area. Thus in a single section gaps may reflect faithfully what actually happened. One would not expect a marine species to be present through an interval of non-marine sediments . Local gaps are not necessarily due to the incompleteness of the fossil record.

This is one case where the completeness of the fossil record is largely irrelevant . Despite the claims of some evolutionary scientists that relative strati­ graphic position cannot be used to determine ancestor- descendant relationships, it is extremely rare for fossils to be preserved in the wrong se­ quence with respect to the order in which they evolved . This can only happen when two species coexisted . If one became extinct long before the other evolved, there is no way in which they can be preserved in the wrong stratigraphic order (Fig. 5) . So to estimate the adequacy of the fossil record it is only necessary to determine what proportion of all species that ever lived coexisted at any one time . The precise value depends on the distribution of relative survivorship of fossil species, as well as changes in diversity throughout the Phanerozoic . Nevertheless, if it is assumed that, on average, species existed for 6 million years, and the Phanero­ zoic was 600 million years long, published estimates of Phanerozoic diversity patterns indicate that approximately 3% of all Phanerozoic species co­ existed at any one time (Paul 1985) . Thus in 97% of possible comparisons there is no possibility what­ soever of species being preserved in the wrong order. Furthermore, the probability is always greater that the correct, as opposed to incorrect, sequence will be obtained even in the 3% of cases where it is possible the order might be wrong. These percent­ ages are not affected at all by the completeness of the fossil record . Indeed if it consisted of just two B

D

3 C

2 A

1

Fig. 5 Total original ranges over three time intervals (1 - 3) for two pairs of species. As the ranges of A and B do not overlap there is no chance whatsoever that they could be preserved in the wrong stratigraphic order. C and D did coexist (at time 2) and so could possibly be preserved in the wrong sequence . However, note that the probability of this occurring is low and that as soon as a single example of species C is found from time 1 , the possibility ceases to exist . (From Paul 1985 . )

3 . 12 Completeness of Fossil Record fossils, the probability is overwhelming that they would be preserved in the correct sequence .

References Anders, M . H . , Krueger, S.W. & Sadler, P.M. 1987. A new look at sedimentation rates and the completeness of the strati­ graphic record. Journal of Geology 95, 1 - 14. Hay, W.W. 1972. Probabilistic stratigraphy. Ee/ogae Geologicae He/vetiae 65, 255 -266 . McKinney, M . L . 1986 . Estimating volumetric fossil abun­ dance from cross-sections: a stereological approach . Palaios 1, 79 - 84.

303

Paul, e . R . e . 1982. The adequacy of the fossil record. In: K.A. Joysey & A . E . Friday (eds) Problems of phylogenetic recon­ struction . Systematics Association, Special Volume 21, pp . 75 - 1 17. Academic Press, London and New York. Paul, e.R.e. 1985 . The adequacy of the fossil record recon­ sidered . Special Papers in Palaeontology 33, 7-15. Retallack, G . 1984. Completeness of the rock and fossil record: some estimates using fossil soils. Paleobiology 10, 59 - 78 . Schindel, D . E . 1980. Microstratigraphic sampling and the limits of palaeontologic resolution . Paleobiology 6, 408 -426 . Schindel, D . E . 1982 . Resolution analysis: a new approach to the gaps in the fossil record . Paleobiology 8, 340- 353 . Shaw, A . B . 1964. Time in stratigraphy. McGraw Hill, New York.

4

PALAEOECOLOGY

A percoid Mioplosus labracoides with a partially ingested small herring Knightia eocaena from the Eocene Green River Formation, x

0 . 4 . (From Grande, L. 1984 . Bulletin 63 (2nd edn) . Geological Survey of

Wyoming, with permission . )

4 . 1 Morphology L. L U G A R

such as load bearing in structures that are subject to forces which may cause breakage. Such approaches attempt to determine how systems respond to the constraints or limitations on design imposed by forces generated in the environment. The develop­ ment of new techniques, using equipment such as force transducers, strain gauges, and high speed filming, have improved the resolution and accuracy of measurements and have increased understanding of mechanical structures made of bone (Lauder 1981). The problems that these studies investigate such as feeding at the air - water interface, or the use of filters in suspension feeding - are useful in palaeobiology as they address generalized problems about constraints or limitations that the environ­ ment places upon the functioning of organisms. Although none is directly applicable to fossils, these techniques can guide inquiry by illustrating the limits placed on function by the demands of the environment, and by exposing the assumptions underlying hypotheses of function. In this way they can help in the design of experimental methods that are applicable to fossils. Palaeomorphologists can make physical models of fossil animals, and then experimentally test hypotheses about function and the adaptive qual­ ities of structures of interest. Kingsolver & Koehl (1985), for example, constructed physical models of Palaeozoic insects and tested hypotheses about the possible uses of wings for gliding, thermo­ regulation, and stabilization during flight by placing these models in various regimes in a wind tunnel. They were able to differentiate between the relative effectiveness of long versus short wings for these properties, and to suggest that insect wings orig­ inally were subject to selection for thermodynamic qualities and only subsequently used for aero­ dynamically more stable movement (see also Section 1 . 9 . 1) . A classic use of physical models in palaeo­ biology is Stanley's (1975) study of the effect of varying shell shape and surface texture on bur­ rowing in bivalve molluscs. Studies by Kontrovitz & Meyers (1988) on the eyes of ostracodes demonstrate an extremely ef­ ficient use by the eye of downwelling light in the water column. They were able to determine the

Introduction Morphology is the science of describing and analys­ ing form in animals and plants. For palaeobiologists the particular concern is to reconstruct the life form, habitat, ecological role, behaviour, and basic biology of fossil specimens that belong to taxa now extinct. The methodological questions that immediately confront the palaeomorphologist concern the intel­ lectual tools that will reliably guide interpretation of form and function, especially when living speci­ mens of related taxa do not exist. As with any morphological research, the palaeobiologist must describe or characterize the form of interest, set the boundaries of the structure to be analysed, form hypotheses about the function(s) of the feature in question, and determine what other elements of the fossil record are similar. The current upsurge in vigour of morphological research derives from advances of theory and methodology in all of these areas. Morphological research on extant taxa can be central to interpreting the functions of fossil struc­ tures by providing well constructed models of structural systems that may give clues to the func­ tioning of fossil organisms. Liem & Wake (in Hildebrand et al . 1985) classified current morpho­ logical research into two major approaches, the first asking questions about current function and the second about historical origin, transformation, and maintenance of morphological structures.

Experimental approaches to morphology Experimental approaches can be used to investigate how structures work for living organisms in the environments in which they are presently found. The techniques used by researchers in this area e.g. by Bramble & Wake, in a study (in Hildebrand et al. 1985) of the function of the lower tetrapod jaw in feeding - help to identify the elements of the skeleton or musculature involved, measure the forces they exert, and describe the way that these forces help effect food capture (Fig. 1). Experimental approaches can also focus o n speci­ fic mechanical problems faced by skeletal systems,

307

308

4 Palaeoecology STR U CT U RA L N ETWO R K

U p pe r jaw p ro t r u s i o n

M ax i l l a

Mand i b l e

�

Upper j a w p rot r u s i o n M ax i l l a

-@

G e n e ra l ized p e rco i d

Cichlid

Fig. 1 Mechanical pathways which affect upper jaw protrusion in cichlid fish as compared with the generalized percoid. The research identified the morphological elements that are involved in the protrusion and illustrated the mechanical pathways controlling jaw movement, and the forces involved in this movement. In generalized percoids, two biomechanical pathways mediate upper jaw protrusion: mandibular depression and maxillary rotation (pathways 1 and 2) . Suspensorial movement influences the upper jaw by an intermediary articulation with the maxilla (pathway la). In cichlid fishes, suspensorial movements can effect upper jaw protrusion independently of maxillary motion and the suspensorium has thus been mechanically decoupled from the maxilla (pathway 3) . An additional mechanical pathway controlling upper j aw protrusion, neurocranial elevation by the epaxial muscles (EM), is also present. A consequence of the decoupling of suspensorial movement (elimination of pathway la) and the increase in number of kinematic pathways controlling the function of upper j aw protrusion is greatly increased functional versatility and increased diversity of jaw morphology in comparison to generalized percoid lineages. This example illustrates both decoupling of a primitive biomechanical link (pathway la), and a proliferation in the number of mechanical pathways controlling a function . Both modifications correlate with an increase in diversity of the structural network. Al part Al of the adductor mandibulae muscle, LAP levator arcus palatini muscle, r realization of the function of upper jaw protrusion by the indicated pathway. =

maximum water depth at which light could be distinguished from dark by the ostracode eye, based on physical equations and elements of eye mor­ phology . This analysis can be extended to eye struc­ tures in fossils and, through the examination of fossil morphology, potentially can be used for palaeobathymetric determination and for estimat­ ing habitat light conditions. This experimental approach corresponds to the equilibrium approach which, as characterized by Lauder (1981), assumes that the organisms studied are optimally designed for function in their present environment. Experimental approaches are widely used to reveal the biomechanical attributes of sys­ tems, and to determine current function . The dem­ onstration that a structure helps an organism solve problems connected with its present mode of life is useful in establishing its 'adaptedness' in the orig­ inal sense of well designed connection between

=

=

organism and environment (Fisher 1985; Section 2.9). However, demonstrating the present function of a structure does not necessarily establish the evolutionary adaptedness of the character, for it does not demonstrate that the structure was shaped by natural selection for its present function. Theoretical criticisms of the equilibrium approach centre around difficulties in defining optimality, in choosing criterion scales whose maxima or minima provide a metric for discussion of optima, and in the existence of constraints of a historical nature that limit achievement of optima through natural selection (Lewontin 1987) . Biologically oriented criticisms of optimality centre on the historical and genetic barriers to the potential realization of opti­ mal form . Such barriers include possible lack of necessary genetic diversity in populations, con­ straints imposed by the requirement for a functional developmental architecture, and the disruptive ef-

4 . 1 Morphology fects of stochastic processes in evolution (Gould & Lewontin 1979) . In addition, the realization that structures often have multiple functions, that function may change during the life of the individ­ ual, and that selection pressures may vary during ontogeny, has led to an increased understanding of the complexity of testing for adaptedness and optimality (see also Section 2 . 9) . Some workers have undertaken careful experi­ mental designs that attempted to identify and evaluate the importance of various selective forces acting on a particular structure or pair of structures . Lowell (1987) used safety factor analysis to examine shell strength and foot tenacity of intertidal gastro­ pod limpets, to identify the importance of selection for one factor on the achievement of effective per­ formance in the other factor. Lowell's results indi­ cated that two developmentally and functionally distinct structures, the foot and the shell, are quite closely coadapted in limpets from two separate gastropod subclasses (Lowell 1987) . By examining mortality in the field in conjunction with safety factor analysis for these limpets, Lowell identified two potentially important selective pressures: lateral crushing forces generated by fish predators on trop­ ical shores, and prying forces generated by crab and bird predators on both tropical and temperate shores . Although a crucial first step, demonstrating that a morphological structure functions particularly well under specific conditions does not establish conclusively that the structure contributes to differ­ ential survival and reproduction of that animal . Lowell' s inferences about selective pressures on the limpets examined were strengthened by showing through field studies that there are predators active in the habitat capable of inflicting forces on the animals similar to the laboratory-generated forces . Lowell's study identified morphological features, such as a thickened aperture lip on the shell, which may be of use to the palaeontologist in examining the fossil record. However, even demonstrating that a feature is undergoing selection presently does not necessarily elucidate the origin and early evolution of that feature in a lineage . The equilibrium ap­ proach used by Lowell does not explain the origin and original forces shaping the basic limpet shell and aperture form, which appear in the fossil record in the Cambrian, well before the first occurrence of the hypothesized predators, and in a different habi­ tat . Researchers interested in the origin and evo­ lution of morphological features have developed methods to specifically address these questions .

30Y

Phylogenetic approaches to morphology While some workers have focused on the role of natural selection in shaping morphology in response to functional requirements, others have explored the historical or phylogenetic approach - the trans­ formational approach of Lauder (1981) . Here the emphasis has been on understanding the intrinsic factors of structural evolution, within a well sup­ ported phylogenetic context. The transformational approach places features in nested sets within a monophyletic lineage and looks for generalized or emergent properties of functional systems (Lauder 1981) . This allows the construction of testable hy­ potheses about historical patterns of change and about patterns of diversity involving terminal taxa . One research programme for identifying intrinsic elements of design is to examine developmental processes. Evolution produces morphological change by varying particular features of the devel­ opmental pathways of organisms . Research has focused on several major classes of alteration of developmental processes. Changes in the time during development at which a process takes place, heterochrony, have been of central concern to mor­ phological and evolutionary researchers (see Section 3.4) . Alberch et al. (1979) developed a formal model for describing the effects of heterochronic changes in timing on the shape of animals . They identified the beginning and ending of growth of a feature, the rate of growth, and the size of the initial growth area, as being crucial to understanding the relationship between changes in developmental pathway and adult form. Some developmental bio­ logists have begun to look at what Goodwin (1984) called generative paradigms . Here the emphasis is on describing developmental patterns arising from fields of embryonic tissue that specify elements of a structure, such as the developing limb of vertebrates (Fig. 2) . There may be constraints (in a positive sense, i . e . focusing of direction or channelling of developmental possibilities) that arise from limi­ tations on the possible alterations of specifications of patterns of developing limbs or other features (Goodwin 1984) . The effect of theoretical advances in developmental studies has been to provide alternative hypotheses that explain patterns, such as the loss or gain of digits in lineages of tetrapods, and to provide new avenues for experimentation . Within palaeobiology, the transformational ap­ proach can be used to order fossil taxa in nested sets, thereby elucidating structural patterns in the historical appearance of features. This ordering adds

310

4 Palaeoecology

Fig. 2 The contour plots represent the solutions to field equations generated by a model of pattern formation for a hind limb with five digits. They demonstrate the possibility of generating specific descriptions of activity in limb buds which will describe patterns of organization and constraints on the possible forms which the bud can generate. (Reprinted by permission of John Wiley & Sons, Ltd, from Evolutionary theory: paths to the future, ed. J.W. Pollard, © 1984.)

precision to the imputation of homology, where a structure in a fossil taxon may be judged to share the known function in a Recent form due to pro­ pinquity of relationship. Palaeobiological inquiry can add taxa to monophyletic evolutionary groups under study, which may provide new characters, characters in new complexes, or states not present in Recent taxa.

The uses of analogy in palaeobiology For many organisms of interest to the palaeobiol­ ogist, no modern homologue is available. Indeed, one of the most interesting and challenging tasks in palaeobiology is the interpretation of the rich fossil record of forms having bizarre and unusual mor­ phologies (Hickman 1988; Section 5 . 2 .5) . This study should be conducted not simply as a de­ scription of peculiar structures but also as a search for recurring patterns in 'fundamental attributes such as size, shape, symmetry, and ratios of surface area to volume' (Hickman 1988) . When no modern homologues are available as guides to function or behaviour, analogy is invoked. Several conceptual tools have been developed within palaeontology to

increase the rigour and explanatory range of mor­ phological research. These include the paradigm method of Rudwick (1964), Seilacher's Konstruktions­ morphologie (1973), theoretical morphology (e. g. Raup 1966), and the increased possibility for precision and analytical manipulation that comes from modern morphometries .

The paradigm method. The paradigm method was elucidated by Rudwick (1964) as an attempt to for­ malize the use of analogy in explaining the function of a structure or element of structural design. The paradigm method is used to try to place the organ­ ism into an environment as a working machine. In Rudwick's formalization, the paradigm is the form of a structure that will most efficiently carry out the hypothesized function(s) of the biological structure of interest, provided that construction is of bio­ logical materials appropriate to the organisms being studied. The paradigm method is most useful when several functional hypotheses are being tested. Thus the application of the method proceeds by postu­ lating several functions for a structure, specifying an optimally efficient form for each function, and examining the degree of resemblance between the

311

4 . 1 Mo rphology form possessed by the organism and those postu­

duction of specific forms . These categories have

lated by the researcher . The paradigmatic form with the closest fit to the real form may be judged to

great value as a heuristic device for sharpening awareness in the researcher of 'what types of in­

represent the actual function of the structure . The

formation prevail' in the production of a particular

ideal forms that serve as the source of the analogy

form (Hickman 1988) .

are usually chosen from classes of machine, such as

When applied to particular systems, Seilacher's

pumps, levers, or bridges, for which mechanical

categories may be extended or modified to suit the

engineering can be used to specify the optimal

needs of the system under analysis . Thus Hickman

(1980) used phylogenetic, mechanical, ecological,

design for accomplishing a specific task . The paradigm method has been criticized because

degenerative, and constructional factors in the analysis of form and

question, and because it assumes only one function

function in the molluscan radula (a toothed tongue

it assumes optimality of design for the feature in

programmatic,

maturational,

for a structure. It also uses chiefly mechanical anal­

exhibiting

ogies for function, thus ignoring other sources of

This expanded list of factors arises from the reali­

substantial

morphological

variation) .

insight such as architecture, communication sys­

zation that certain aspects of morphology are best

tems, transportation systems, etc. (Hickman 1 988) .

examined in a non-evolutionary context, so as to

Further, although it can specify optimality of design

reveal important information about the production

in the ideal form, there are no rigorous criteria for

of form that might otherwise be obscured. The teeth

the minimum resemblance between paradigm and

of the molluscan radula, for example, are produced in a form that requires shaping by use before

organism needed to justify the imputed function (Signor 1982) . However, Fisher (1985) has shown how the method can be translated into a problem in

achieving the most effective functional form. A pencil, which comes from the factory in a form

Bayesian inference, and he has also elucidated the

requiring

use of tests of minimally sufficient or threshold

provides an analogy .

modification

before

it

can

be

used,

conditions for achieving a particular functional ef­ Theoretical

morphology

fect . Further, if divergent hypotheses of function

Theoretical morphology.

are made, with different ideal forms described, then

uses mathematical description of the parameters

observation may reveal which prediction of form is

that control shape and its alteration to prescribe the

actually realized by the organism .

domain of form that can result from transformations of the original specification. Raup ( 1966) used four

Konstructionsmor­

parameters to establish the overall form open to

morphology)

was

conispiral shells . These four elements - the shape

developed by Seilacher (1973); it enables the mor­

of the generating curve, the rate of expansion of that

Constructional phologie

(or

morphology. constructional

phologist to speculate about function in a broad

curve with respect to revolution about its axis, the

framework that takes into account both evolutionary

position and orientation of the curve in relation to

history and ontogenetic problems . Seilacher cited

the axis, and the rate of translation around the axis -

three major factors that must be recognized in the

establish

analysis of form . These are:

shells .

(1)

the functional el­

the

basic

morphospace

for

conispiral By generating all possible outcomes of

(2) the fabricational or

changes in these parameters, Raup analysed the use

architectural element (Bautechnischer Aspekt); and

(3) the phylogenetic element (Historischer Aspekt) .

of form in molluscs in terms of which possibilities have been realized through the evolution of actual

These factors summarize the action of various forces

organisms . These areas of morphospace can be

ement (Adaptiver Aspekt);

and constraints on the production of form . The

compared with those areas that are occupied . This

functional element describes the action of natural

allows hypotheses about function, or insights into

selection in shaping a structure for efficient use .

structural or design constraints, to explain why

The fabricational element refers to the developmen­

certain forms have not evolved .

tal patterns and processes that produce an individ­ ual organism . The phylogenetic element refers to

Morphometries.

the evolutionary history of a taxon . The interaction

developing very rapidly. The use of techniques

of these forces produces form, constrained by the limitations they impose . A primary goal of con­

The subject of morphometrics is

such as the theta-rho analysis of Siegel & Benson

(1982) to describe areas of shape that differ between

structional morphology is the elucidation of the

two forms, while simultaneously identifying the

relative importance of these elements in the pro-

areas that remain constant, have greatly improved

4 Palaeoecology

312

801.

Plethodontidae

*

Ane.

Paed o m o rp h

PREMAX I L LARY EVO L U T I O N

r-,.------.,

Pera m o r p h

D i rect d eve l o p m e n t

... T ra n s fo r m a t i o n

O n to g e n y M et a m o r p h o s i s

La rva

�

Ad u l t

( e m b ryo) A n c e s t ra l

o n t o g e ny

Fig. 3 The use of a phylogenetic hypothesis as the framework onto which the recurring forms of the pre-maxilla of plethodontid salamanders could be mapped illustrates the use of several lines of morphological evidence to elucidate an evolutionary question. The ancestral ontogeny is indicated at the base, with a bipartite premaxilla persisting throughout ontogeny (hollow arrow) . Synapomorphies (Section 5.2 .2) are indicated in boxes. Evolutionary transformations (solid arrow) occur within some of the synapomorphous states . The unipartite premaxilla typically divides during metamorphosis or early ontogeny, but evolutionary changes causing unipartite premaxillae to appear in adults have occurred at least five times, two by peramorphosis and two by paedomorphosis (Section 2 . 4) . D subfamily Desmognathinae, Hem . Hemidactylium, Gyr. Gyrinophilus, Eur.* all members of the tribe Hemidactyliini except the two preceding genera, Ens . Enstatina, Pie. Plethodon, Ane. Aneides, Hyd. Hydromantes, Bat. 1 Batrachoseps campi and B. wright, Bat. 2 all remaining species of Batrachoseps, Nyc. Nyctanolis; Bol.* all members of the supergenus Bolitoglossa except Nyctanolis. =

=

=

=

=

=

=

=

=

=

=

=

the ability of morphologists to study transform­ ations of form during ontogeny and throughout evolutionary sequences . The use of computer­ assisted methods of image capture, and of precise

measurements of such standard morphological determinations as lengths, widths, perimeters, and areas, has greatly increased the speed and accuracy with which measurements may be made and has

4 . 1 Morphology also speeded processes such as digitization to allow the compilation of larger databases (see Section 6.1).

Conclusions The combination of several lines of approach to problems of evolutionary morphology seems likely to yield results that will make morphological re­ search interesting to researchers in a wide array of fields, such as evolutionary biology, developmental biology, and ecology. Wake & Larson (1987) ana­ lysed the evolution of the skeletal and muscular elements of the autopodium, premaxilla, and feeding structure of plethodontid salamanders by using a combination of structural and neo­ Darwinian approaches . They viewed individual development as a closed set of epigenetic transform­ ations that could be used to predict a limited num­ ber of possible forms open to the organism, and they examined the production of these forms by using cladistic and populational genetic analysis of the history and population structure of natural populations . They were thereby able to identify design constraints on the salamander feeding struc­ ture, and illustrate its achievement in several living salamander genera (Fig. 3) . They illustrated the fre­ quent occurrence of heterochronic changes within the lineages examined and built up a hypothesis for the role of various forces affecting the morphology of plethodontid salamanders in the shaping of individuals and for the deployment of that shaping in evolutionary time . Morphologists have a wide array of conceptual tools and experimental procedures available to them for the analysis of form, and the present flourishing of research into morphology reflects this . Evo­ lutionary biology and palaeontology have con­ tinued to develop vigorously and an understanding of the ecological role, evolutionary history, and strati­ graphic significance of fossil forms is still an area of active research. Thus morphology continues to play an important role in palaeobiology.

References Alberch, P., Gould, S.J., Oster, G . & Wake, D. B. 1979 . Size and shape in ontogeny and phylogeny. Paleobiology 5, 296- 317.

313

fisher, D . e . 1985 . Evolutionary morphology: beyond the analogous, anecdotal, and the ad hoc. Paleobiology 11, 120 - 138 . Goodwin, B . e . 1984. Changing from a n evolutionary t o a generative paradigm in biology. In: J.W. Pollard (ed . ) Evolutionary theory: paths to the future, p p . 99 - 120. John Wiley & Sons, Chichester. Gould, S.J. & Lewontin, R.e. 1979 . The Spandrels of San Marcos and the Panglossian paradigm: a critique of the adaptationist programme. Proceedings of the Royal Society of London B205, 581 -590. Hickman, e . S . 1980 . Gastropod radulae and the assessment of form in evolutionary paleontology. Paleobiology 6, 276296 . Hickman, e . S . 1988 . Analysis of form and function in fossils . American Zoologist 28, 775 - 793. Hildebrand, M., Bramble, D . M . , Liem, K.F. & Wake, D . B . (eds) 1985 . Functional vertebrate morphology. Belknap Press, Cambridge, Ma. & London. Kingsolver, I . G . & Koehl, M.A.R. 1985 . Aerodynamics, thermoregulation, and the evolution of insect wings: differential scaling and evolutionary change . Evolution 39, 488 - 504 . Kontrovitz, M. & Meyers, J .H. 1988. Ostracode eyes as paleo­ environmental indicators: physical limits of vision in some podocopids. Geology 16, 293 -296 . Lauder, G.V. 1981 . Form and function: structural analysis in evolutionary morphology. Paleobiology 7, 430 -442 . Lewontin, R . e . 1987. The shape of optimality. In: J. Dupre (ed . ) The latest on the best; essays on evolution and optimality. MIT Press, Cambridge, Ma. Lowell, R.B. 1987. Safety factor analysis of tropical versus temperate limpet shells: multiple selection pressure on a single structure. Evolution 41, 638 - 659 . Raup, D . M . 1966 . Geometric analysis of shell coiling: general problems . Journal of Paleontology 40 , 1 1 78 - 1 191 . Rudwick, M.J. 1964. The inference of structure from function in fossils. British Journal for the Philosophy of Science 1 5, 27-40 . Seigel, A.F. & Benson, R.H. 1982. A robust comparison of biological shapes . Biometrics 38, 341 - 350. Seilacher, A. 1973 . Fabricational noise in adaptive mor­ phology. Systematic Zoology 22, 451 -465 . Signor, P.W. 1982 . A critical re-evaluation of the paradigm method of functional inference. Neues Jahrbuch fUr Geologie und Paliiontologie, Abhandlungen 164, 59 -63. Stanley, S.M. 1975. Adaptive themes in the evolution of the Bivalvia. Annual Review of Earth and Planetary Sciences 3, 361 - 387. Wake, D . B . & Larson, A. 1987. Multidimensional analysis of an evolving lineage . Science 238, 42-48 .

4 . 2 Composition and Growth of Skeleton B . RUNNEGAR

almost insoluble in water, and non-toxic, but each is also soft and brittle and most are relatively dense . How then are these substances used to make size­ able, strong, and light-weight skeletal structures, and when did these innovations first take place? To a first approximation, most skeletons may be described as stiffened walls, scaffolds, or shells. Stif­ fened walls (such as the chicken eggshell) are min­ eralized all at once after they have been shaped by soft tissues, whereas shells are produced over a long period of time by incremental growth. Both kinds of structure may coexist in a single skeleton: the coiled conch of Nautilus is a classic shell but its internal septa are better described as stiffened walls . Simi­ larly, the echinoid test is best modelled as a stiffened wall or 'Pneu' (Seilacher 1979), although its com­ ponent plates display the incremental growth that is typical of shells . Scaffolds differ from both walls and shells in being static or dynamic structures formed of linear or planar subunits . The calcareous and siliceous spicular skeletons of sponges and the limbs and rib cages of vertebrates are scaffolds in this sense . They provide structural support but do not enclose the soft tissues and hence are of little use as armour. In contrast, many skeletons are hollow structures in which organisms reside . These enclosures can be built in two main ways : either by assembling pre­ fabricated modules in the shape required, or by growing the mineral inwards from a preformed substrate that surrounds the body. Both of these methods of construction have severe geometrical constraints. Opaline silica has had limited potential as a skeletal material except in microscopic organisms (radiolarians, diatoms, silicoflagellates), because of its non-crystalline, glassy nature and intracellular mode of formation. In contrast, calcium compounds form anisotropic crystals that may be shaped and assembled in a variety of ways by habit-modifying macromolecules (Mann 1988) . A few tiny organisms can make their skeletons from a small number of single crystals, but this method of construction is not available to sizeable organisms because large crystals are difficult to grow, mechanically weak, and unsuitable in shape . Most crystalline skeletons

Introduction Mineral skeletons appeared abruptly about 550 Ma in a great variety of different kinds of organisms . Prior to this time all living creatures used hydrostatic forces constrained by soft or flexible structures to shape their bodies . With the invention of mineral­ ized skeletons, new types of body plans became possible and the conspicuous fossil record of the Phanerozoic began. Many different kinds of amorphous or crystalline mineral compounds are formed biologically (Lowenstam 1981 ) . These compounds are the building-blocks of rigid skeletons, but they also serve to rid cells of unwanted salts, to store useful elements (such as iron and phosphorus), and to act as components of sensory organs that are used for sight, balance, and navigation . In sizeable animals these functions are clearly discrete and are often performed by different kinds of biominerals . For example, some birds have phosphate endoskeletons, carbonate eggshells and gravity sensors, and a navigation system that depends in, part upon . magnetite . The non-skeletal biominerals represent an insig­ nificant volume of all but the smallest organisms . As a result, they are rarely fossilized and the history of biomineralization is largely the history of min­ eralized skeletal materials . These may be preserved in their original condition or be modified by the chemical and physical processes of diagenesis and metamorphism.

Nature of mineral skeletons Nearly all of the mineral skeletons manufactured by living and fossil organisms are made from one or two common inorganic compounds : calcite (a rhombohedral form of CaC03), magnesian calcite (a solid solution of MgC03 in CaC03), aragonite (an orthorhombic form of CaC03, normally having a small amount of SrC03 in solid solution), apatite (a family of compounds of the general formula CalO(P04MOH,F» and opal (hydrated silica with the general formula [SiOn . OH(4- 2n)]m, where n :::; 2 and m » n). Each of these materials is readily available,

314

4 . 2 Composition and Growth of Skeleton

315

are therefore composites of organic polymers inter­ spersed with a mineral phase . These composite materials are better able to resist both plastic deformation and brittle fracture, and they have strengths that are much greater than those of either component alone .

Construction of carbonate skeletons Almost two-thirds of the mineral skeletons formed by living and extinct groups of organisms are com­ posed of the two common polymorphs of CaC03, calcite and aragonite (see also Sections 1 .4, 3 . 8 . 1 ) . Alkaline earth elements with an ionic radius greater than about 0 . 1 nm form orthorhombic carbonates of the aragonite type and thus fit easily into the aragonite lattice . Those with ions smaller than Ca2 + (0. 10 nm) form rhombohedral carbonates of the calcite type and also occur in solid solution in calcite . Thus aragonite commonly contains some Sr2 + (0 . 1 1 nm) but little Mg2 + (0 .06 nm), whereas the converse is true for calcite . Only CaC03 can form both ortho­ rhombic and rhombohedral polymorphs under conditions found at the surface of the Earth . Synthetic calcite usually forms small rhombo­ hedral crystals (Fig. 1) that correspond in shape to the three directions of perfect cleavage found in natural calcites . Similar rhombohedra often line cavities in carbonate rocks but more slowly de­ posited crystals can exhibit other forms . However, the normal habit of natural crystals of inorganic calcite is equidimensional or prismatic . Aragonite crystals are almost invariably fibrous . Each fibre i s pseudohexagonal i n cross-section, being bounded laterally by four faces of one crys­ tallographic from and two of another. The fibres are packed together into radial aggregates, so growth is slow perpendicular to the axis of the fibre and very fast at the tip . Thus, in simple inorganic systems aragonite is characterized by its fibrous habit and spherulitic growth (Fig. 2) . Magnesian calcite also commonly forms fibrous crystals, possibly because the Mg2 + ion poisons the prism faces of the develop­ ing calcite crystals . For the same reason, the presence of Mg2 + may promote the formation of aragonite at the expense of calcite . Single crystals of high-magnesian calcite are used as skeletal modules by calcareous sponges and echinoderms . In the echinoderm skeleton the in­ trinsic weakness of calcite is overcome by the for­ mation of a higher order structure called stereom . In a sense, the echinoderm skeleton may be viewed as a two-phase cubic emulsion of mineral and living

Fig.

1

Synthetic crystals of calcite (greatly magnified) .

2 Two-dimensional computer simulation of the spherulitic growth of aragonite fibres . The program allows equally spaced radial lines to grow from randomly distributed 'nucleation sites' until they intersect. (Program and simulation by F.A. Shaw . ) Fig.

tissue . The interface between the two phases cor­ responds approximately to a surface of zero mean curvature, such as might be formed in a well shaken

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mixture of equal parts of oil and water. The tissue­ filled pores in the echinoderm stereom prevent fractures from propagating through the structure . Some unicellular golden-brown algae manufac­ ture articulated calcareous exoskeletons by prefabri­ cating calcitic plates called coccoliths in intracellular vesicles . Each coccolith is composed of a number of calcite crystals assembled on an organic base-plate or scale in an organized way. The stereochemistry of the scale - mineral interface specifies the orien­ tation of each calcite crystal needed to form the complete assembly. This requires the recognition of the trigonal symmetry of C03 groups within the calcite structure because the hexagonal array of cal­ cium atoms carries insufficient information to specify a unique orientation of the crystal lattice . As a result, most coccoliths have an inherited right­ left symmetry or chirality that is derived from the geometrical properties of calcite. The 'living fossil' Braarudosphaera bigelowi is one of the most spectacular of all coccolith-bearing algae . It encysts within a regular dodecahedron formed of 12 equal-sized calcitic pentaliths (Fig. 3) . Each pentalith is composed of five radial wedges that are single crystals of calcite set at approximately 72° (360°/5) to each other. The fivefold symmetry of each pentalith is not derived directly from the crys­ tallography of the mineral phase, but results from the fact that the 78° angles in the faces of calcite cleavage rhombohedra are almost a fifth of a circle . Many o f the hollow mineralized structures formed by organisms may, at least in principle, be regarded as shells. These are four-dimensional structures in that they are not formed all at once . Instead, growth occurs continuously or episodically for an extended period of time on linear margins or on previously formed surfaces . Most are scale-invariant objects that have the same proportions at all magnifications. The best-known example is the logarithmic spiral of the Nautilus shell, but most other shells, scales, tests, and teeth are built in a similar fashion. The ultimate strength of the construction depends both on its shape and upon the crack-stopping properties of its component materials . In the simplest kinds of shells the mineral is nucleated on the surface of an enclosing membrane (epitheca, periostracum) and it grows towards the living animal in an essentially inorganic fashion. If the mineral is aragonite, magnesian calcite, or apa­ tite, the crystallites will normally be fibrous and the gross structure of the skeleton may consist of a series of spherulitic pseudoprisms (Fig. 4) . Such pseudoprisms are moulded by surface forces rather

Fig. 3 The calcite coccosphere of the alga Braarudosphaera bigelowi is a regular dodecahedron composed of 12

pentaliths, each in turn made from five calcite crystals .

Fig. 4 Computer-drawn model o f the growth o f the outer layer of the Nautilus shell. Aragonite fibres represented by straight lines grow in from the periostracum (curved line) to form spherulites . (Program and simulation by F . A . Shaw . )

than chemical bonds, and they are found in both inorganic and unstructured biological deposits . They begin as hemispherical aggregates that may be nucleated at random on the inner surface of the enclosing membrane, and they grow competitively to achieve a uniform size and polygonal cross­ section by obeying the rules of soap-bubble geo­ metry. Spherulitic microstructures of this type are found, for example, in the walls and septa of coral

4 . 2 Composition and Growth of Skeleton skeletons, in the outer layers of mollusc shells, and in vertebrate eggshells . These simple fibrous microstructures are strong in compression but weak in tension because cracks easily penetrate the layers parallel to the fibres . This defect may be overcome by fibres inclined to the shell surface in one or more orientations, as in molluscan crossed-lamellar shell structure . Another way of making stronger shells is to de­ posit the mineral in thin layers parallel to the shell surface . This method of construction requires a modification of the mineral crystallites to produce shapes that are rarely or never found in non­ biological systems . Molluscan 'mother-of-pearl' (nacre) and its calcitic equivalents are good examples of such layered carbonates . The great strength of nacre allows Nau tilus to inhabit depths of 500 - 600 m where the water pressure is about 60 pascals . The spherulitic aragonitic prisms of the outer layer of the Nautilus shell present the {00l } ends of innumerable fibres to the secreting surface of the mantle . The fundamental difference between the unmodified aragonite fibres and the flat crystals of the nacreous inner shell layers lies in a difference in habit not form. Both kinds of crystals are bounded by equivalent faces, but in nacre growth on {00 l } i s very slow, whereas in the fibres i t i s very fast. It seems likely that proteins rich in aspartic acid residues may be involved in limiting growth on {00 l } in aragonite and stereochemically compar­ able surfaces in calcite. Proteins of this kind have been isolated from the organic matrices of a great variety of skeletal carbonates . They are believed to occur as regular, two-dimensional networks (�­ sheets), to bind calcium, and to have negatively charged amino acids spaced so as to match the arrays of calcium atoms in the surfaces of layered carbonates, such as nacre (Mann 1988) . As the genes for these simple repetitive proteins could have arisen de novo on more than one occasion, it is likely that layered structures developed rapidly and conver­ gently from primitive fibrous ones in a number of different lineages .

Other kinds o f skeletons and the history of biomineralization As a skeletal material, calcium phosphate has proved most successful as either dermal armour or internal support. As a result, most phosphate skeletons con­ sist of a number of different parts (bones, teeth, sclerites, etc . ) that may dissociate and disperse after death. Reconstruction of the whole skeleton, or more

317

generally the scleritome, presents particular prob­ lems for palaeontologists (Bengtson 1985). Little is known about the mechanism of formation of phosphatic skeletons in animals other than ver­ tebrates where the mineral is intimately associated with the proteins collagen and osteocalcin. There is increasing evidence that the y-carboxyglutamic acid side chains of the osteocalcin molecule are respon­ sible for the mineral -protein interaction, and that the role of collagen is to provide a structural frame­ work. A similar situation appears to occur in mollusc shells where glycine-rich proteins that are insoluble in ethylenediaminetetraacetic acid (EDTA) seem to act as the foundation for EDTA-soluble proteins that are rich in aspartic acid residues (Mann 1988) . In both cases the structural protein acts as the energy-dissipating component of the mineral­ matrix composite in addition to providing a sub­ strate for subsequent mineral growth . It is probable that a comparable organization is to be found in many c [her kinds of carbonate and phosphate skeletons . Many kinds o f skeletons may preserve historical information about the ontogeny of the owner and the conditions under which it lived, because they are continuously modified during life . Vermeij (1970) has made the distinction between permanent skeletons that are retained throughout postlarval life and transient skeletons that are shed period­ ically. The former may be secondarily remodelled by normal or pathogenic processes; the latter record snapshots of the ontogeny and are particularly characteristic of the Arthropoda. Persistent incremental growth, as in tree trunks, shells, and open-rooted teeth, produces skeletons that may be viewed as continuous environmental recorders (Jones 1983) . Successive variations in the thickness of growth increments have been used with varying degrees of success to estimate individ­ ual age and growth rates, analyse population struc­ ture, understand local environmental conditions, and provide empirical measures of past day length and other geophysical phenomena. Ontogenetic changes in the isotopic, elemental, and minera­ logical composition of mollusc shells are increasingly being used for environmental analysis, as new analytical techniques allow the sample size to be reduced to growth increment scale . The discovery that early phosphate or carbonate cements may have replicated the fine structure of skeletal minerals altered by subsequent diagenesis has provided new insights into the early history of biomineralization (Section 1 .4) . Almost all of the

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known varieties of skeletal minerals and most of the different kinds of mineral skeletons appeared within a few tens of millions of years at the beginning of the Phanerozoic. Innovations such as molluscan nacre, echinoderm stereom, and the characteristic pris­ matic calcite of the shells of articulate brachiopods were being manufactured by at least the Middle Cambrian. Hardly any new types of skeletal ma­ terials were evolved after the Cambrian and the only kinds of mineral skeletons that appeared during the invasion of the land were the carbonate eggshells of snails and vertebrates. Thus, although new kinds of organisms began to build mineral skeletons in post-Cambrian time (corals, bryozoans, calcareous and siliceous plankton, etc.), they used pathways pioneered previously by cyanobacteria,

eukaryotic algae, animal-like protists, and a large number of metazoan phyla.

References Bengtson, S. 1985. Taxonomy of disarticulated fossils. Journal

of Paleontology 59, 1350- 1358. Jones, D . S . 1983. Sclerochronology: reading the record of the molluscan shell. American Scientist 71, 384-391 . Lowenstam, H.A. 1981 . Minerals formed by organisms. Science 211 , 1 126- 1131 . Mann, S. 1988. Molecular recognition in biomineralization.

Nature 332, 119- 124. Seilacher, A. 1979. Constructional morphology of sand dollars. Paleobiology 5, 191 - 221 . Vermeij, G.]. 1970. Adaptive versatility and skeleton con­ struction. American Naturalist 104, 253-260.

4 . 3 Biomechanics P . A . SELDEN

Introduction Biomechanics is the application of mechanical prin­ ciples to the study of organisms . In palaeontology, only recently have sufficient biomechanical studies accumulated to constitute a bibliography of the subject. These studies span almost the entire range of taxa; their objectives are usually functional mor­ phological and commonly, but not necessarily, quantitative . Conversely, quantitative studies using mathematical or physical principles (e .g. growth form in Bryozoa or vision in trilobites) are not necessarily biomechanics . The major contribution which biomechanics makes to palaeontology is in testing hypotheses of functional morphology that are based on deduction from morphology or external factors, such as sediment, associated biota, or distri­ bution. Biomechanics can be a powerful tool in hypothesis testing, but quantitative results, even on living organisms, must be interpreted with caution because of the inherent complexity of the natural world . Undoubtedly the most important textbook on biomechanics is that by Alexander (1983) and his chapter headings are used here as a basis for

grouping examples of the uses of biomechanics in palaeontology .

Strength An important branch of biomechanics investigates the structural design of organisms, and in particular the properties of the materials of which plants and animals are made (Wainwright et al . 1976) . The common questions asked are about the strength of biological materials under stress, i . e . subject to a force, usually gravity, or a current flow in a static situation or during movement . There is considerable overlap here with constructional morphology (Section 4 . 1 ) . Biological structural materials are usually com­ plex, since they have to operate in a variety of mechanical environments and also perform other feats, like growing. They are mainly composites, good examples being wood, arthropod cuticle, and echinoderm stereom and stroma. Such materials are very resistant to fracture and other forms of failure because they combine both rigid and elastic ma­ terials, and laminates are used extensively for their crack-stopping properties . It is, of course, almost impossible to study the biomechanics of fossils

4 . 3 Biomechanics with soft skeletons . On the other hand, it may be as easy to investigate the mechanical properties of rigid, calcareous fossil skeletons as those of their living relatives . As well as the building materials themselves, the architecture of plant and animal structures is ex­ tremely important for maximizing strength over energy expenditure . In general, tubes are as efficient as, but less costly than, solid beams, which is one reason why bones, arthropod limbs, bicycle frames, and many plant stems are hollow cylinders . There are optimum materials and designs, for example for cylinders required to support heavy, static loads, those which act as levers, and those which suffer heavy impacts . The principles of beam theory are relatively straightforward and have been used in a number of palaeontological analyses with en­ lightening (but perhaps not surprising) results . As this point it is necessary to mention scaling (see McMahon & Bonner 1983) . In many palaeobio­ mechanical studies either the aim of the work or a consequence of it involves consideration of a range of sizes of organisms. Dinosaurs are a good example . Large terrestrial animals must have disproportion­ ately thicker limbs than their smaller relatives, or minimize the stresses involved in walking. The reason for this is that cross-sectional area of the limbs is proportional to [body weight] o . 67 whilst the stresses due to gravity are proportional to [body 33 weight] o . . Apatosaurus was probably quite capable of walking without the aid of water buoyancy, provided it did not indulge in acrobatics . Similarly, Dalingwater (see Briggs et al. in Rayner & Wootton 1991) investigated whether eurypterid arthropods (especially the large Carboniferous forms) could have walked on land, using living Limulus for comparison . Limulus can walk on land, even though it is an aquatic animal, but if the cuticle of the giant Carboniferous eurypterid Hibbertopterus had the same Young's modulus (a measure of elasticity) as that of Limulus, it is unlikely that the latter animal could have done so . A particular problem for arthropods on land is moulting; Dalingwater found that even a small Limulus is unable to support itself out of water in its soft, newly-formed cuticle . His calculations used simple expressions for buckling under static axial load, on the basis that if failure resulted under these conditions, then walking, with its associated greater, non-axial stresses, would be impossible . Arthropod podomeres are hollow cylinders, the axial lumen housing the muscles which operate them, so the thickness (t) of cuticle cannot equal the

319

radius (r) of the cross-section (r : t *- 1 ) . This is another constraint on the size of terrestrial arthro­ pods . In flying animals (Section 1 .9) and swaying plant stems, the problem is less the result of weight and more that of failure by bending. Flight im­ poses a number of constraints, particularly on large animals like giant pterosaurs (Quetzalcoatlus from the Upper Cretaceous of Texas had a wingspan of 12 m, and was thus the largest flying creature ever) . r : t ratios below about eight give considerable strength against impact but are heavy. Where r : t exceeds eight there is considerable weight saving, but brittle fracture is a problem, and buckling be­ comes a problem when r : t exceeds 15. So how do large pterosaurs combine lightness with strength in their wing bones? (1) Their bones are laminated to lessen cracking under impact or load; (2) larger pterosaurs have higher r : t ratios for lightness (the bone thickness is the same as in small ones but the lumen is wider); and (3) to prevent buckling, a number of devices (Fig. 1) are employed which effectively lower the r : t ratio and produce strong 'T' sections without adding a significant weight of bone . Geological evidence shows that, not surpris­ ingly, giant pterosaurs, like large birds, lived in open treeless surroundings where impact damage was minimized . At the other extreme, low r : t ratios are useful in situations where impacts are common. Kitchener (in Rayner & Wootton 1991) used beam theory to show that the r : t ratio of the cross-section of the proximal part of Irish Elk antlers was far smaller than would be expected if the antlers were used for

Fig. 1 A, Cross-section of a tube showing radius (r) and thickness (t); r : t 2.4. B, Thick-walled section near base of Irish Elk antler; r : t 3. C, Section of first phalanx of pterosaur, showing devices for combining strength and lightness: thin walls, triangular section with thickened corners (commonly hollow), struts, and spongy bone layer; r:t 1 1 . All are diagrammatic and not to scale . =

=

=

4 Palaeoecology

320

display alone, and since antlers are shed annually they are a significant expense . Antlers of other Old World deer are used for fighting among males vital for the breeding success of the species. The high r : t ratio, together with the preferred orienta­ tion of osteons in the maximum impact direction of the proximal antler bone, is good evidence that fighting was the real function of Irish Elk antlers .

Force and energy The force (in newtons) which Irish Elk antlers needed to withstand was that of an equal but op­ posing weight of stag colliding at the same rate of 2 deceleration (500 kg X 30 m/s 15 000 N per antler) . In this situation the force is maximum in the direction of motion of the deer. In a lever system, such as when muscles move a bone or an arthropod podomere, the resultant force is in a different direc­ tion to that of the muscle contraction. Alexander (1983, p . 5) gave an example of how some knowledge of the action of levers helps to explain the evolution of the mammalian jaw articulation from that of a primitive reptile . Claws (chelae) of crustaceans and chelicerates work in a manner similar to that of mammalian jaws . In a lever system, the ratio result­ ant force : applied force (F2 : F1) is known as the mechanical advantage (MA), and L1 : L2 is the vel­ ocity ratio (VR) (Fig. 2) . A high MA or VR (i. e . close to 1) provides strong but slow movements; in con­ trast, a low MA or VR leads to weak but fast move­ ments with the same power input. These simple relationships are useful for understanding the func­ tion of chelae or jaws in fossils, such as eurypterids (Selden 1984) . =

�--_ F ,

Fig. 2 Mechanics of cheliceral claw of a pterygotid eurypterid; VR (L1 : L2) 0.2 for tip of movable finger, therefore MA (F1 : F2 ) is also low, and adapted for fast capture of prey. Prey inserted into claw at X could be sliced with high MA . =

Similar principles apply to walking: long legs are good for fast running, short legs for strong pushing. The analysis of walking is complex (e . g . for arthro­ pods see Briggs et al. in Rayner & Wootton 1991) . For example, a surprising but useful source of infor­ mation on the biomechanics of walking in fossils is their tracks . Stride length, and hence leg length, can be measured from footfalls . Alexander (1983, p . 35) used the concept of kinematic similarity, which allows extrapolation from the scale of a small animal to that of a dinosaur provided that their Froude numbers are the same . Froude number, like Rey­ nolds number (see later), is a dimensionless quan­ tity, u 2 /gl , where u, g and I are a velocity, acceleration due to gravity, and a length respectively. Alexander calculated the speeds of some dinosaurs from Texas and found that the biped walked at c. 2.2 m/s while the quadruped strolled at c. 1 m/s; both are reason­ able human walking speeds.

Pressure, density, and surface tension Hydrostatic skeletons in plants and animals come under this heading, but the fossil record can tell us little about them . Surface tension may seem to be a phenomenon which cannot be studied easily in fossils, yet it is important wherever biological tissue encounters an air-water interface (e . g . in lungs) . Alexander (1983, p . 176) discussed the importance of surface tension in the operation of plastrons in aquatic insects and mites; the surfaces of eurypterid respiratory organs resemble those of plastrons in morphology, but not in size, and therefore could not have worked in the same way. Buoyancy is another hydrostatic phenomenon, and has been of interest to cephalopod palaeo­ biologists in particular. Fish and endocochleate (internal-shelled) cephalopods have nearly coinci­ dent centres of buoyancy and mass, which allows for accurate swimming and controlled manoeuvr­ ability. This was probably true of the belemnites and some straight-shelled ectocochleates as well. The coiled ectocochleate nautiloids and ammonoids, on the other hand, had their centre of buoyancy above their centre of mass. This is inherently more stable when static, but jet thrust sets up a couple which rotates the animal, and a restoring moment is provided by the body mass when the thrust force subsides . A further disadvantage in the cephalopod model of a buoyant camerate shell, counterbalanced by solid or liquid ballast, is that it is costly in energy, both to secrete and to move, in contrast to the fish solution.

4 . 3 Biomechanics Motion in fluids As soon as cephalopods start to move, they experi­ ence a variety of phenomena associated with motion in fluids . The dimensionless number describing kinematic similarity in fluid motion, equivalent to the Froude number where gravity is important, is the Reynolds number (Re) . Two forces which act on objects moving through a fluid, and which are dependent on Re, are lift (L) and drag (D) . These concepts are explained in Section 4.4. In biology, motion of a body through a fluid can initially be classified into swimming (in water) and flying (in air) . Flight is discussed in Section 1 .9; only swim­ ming is reviewed here . Jet propulsion is used extensively by cephalo­ pods; water is drawn into the mantle cavity and then expelled rapidly through the funnel to push the body forward . Broadly speaking, the larger the mantle cavity, the greater the thrust which can be achieved and sustained; this is limited in ecto­ cochleates by the size and buoyancy requirements of the shell . Endocochleates have no such restraint on the size of the mantle cavity. Progression consists of cycles of alternating propulsive jet thrusts (power stroke) and inhalation (recovery stroke) . Such burst swimming may not be as inefficient as it appears, since it is common in fish, and bounding flight is efficient in small birds . Chamberlain (e.g. in Rayner & Wootton 1991) has analysed various aspects of swimming in ectocochleates; in particular, he showed how drag varies with changes in expansion rate, whorl shape, and position of whorls relative to the coiling axis. In general, involute oxycone shells have a lower drag coefficient (and hence were more efficient) than depressed cadicones . In some cases the amount of soft part protrusion has an effect on the drag, and fine ribbing can also reduce the drag coefficient significantly. Using experimental measurements of drag on fossil ammonite shells, calculations of body volumes, and comparison with the rotational moments experienced by living Nau­ tilus, Chamberlain estimated the swimming speeds of these extinct animals . They were undoubtedly poor swimmers in comparison with modern fish . Vertebrates and arthropods swim by one of two methods: axial or paraxial. The former method in­ volves undulations of the body; it is predominant in fish, in which group direct comparison between living and fossil forms can be made . Paraxial loco­ motion is of more interest to palaeontologists because it was used by such extinct forms as eurypterids and plesiosaurs, and involves move-

321

ments of paired limbs to drive the body through the water. There are essentially t� o types of paraxial locomotion: drag-based rowing; and lift-based 'flying', so-called because the mechanical prin­ ciples involved are the same as those in aerial flight (Section 1 .9) . In rowing, the paddles, with high drag, are moved backwards to propel the stream­ lined body forwards; during the recovery stroke, the paddles are feathered to reduce their drag. In subaqueous flight the flipper is moved up and down at right angles to the direction of body move­ ment; the limb's hydrofoil cross-section produces a force, lift, which is directed forwards by rotating the flipper. Lift can be generated on both the up and down strokes, so that forward progression is continuous . At Reynolds numbers below about 102, viscous forces are important, so drag-based rowing mech­ anisms are used by small and/or slow swimmers . Above about Re 5 x 103, inertia dominates, s o it is more efficient to fly, if possible . Eurypterids straddle this Re transition; small species un­ doubtedly rowed (Fig. 3B), but it seems most likely that the large (up to 2 m) pterygotids flew under­ water. The biomechanics of eurypterid swim­ ming was discussed by Selden (1984) and Briggs et al. (in Rayner & Wootton 1991) . Using a simple rowing model, the maximum sustainable speed was calculated at 38 cmls for a 16.5 cm long Baltoeuryp­ terus, which conforms with extrapolations from the swimming speeds of water beetles. Estimates of Re at this velocity give approximately 2 X 104, which is just into the range in which flying should be more efficient, so it is possible that swimming was nor­ mally slower than this, or that constructional mor­ phology was a constraint. Morphology suggests that the paddles of Baltoeurypterus moved in phase, as in water boatmen (e .g. Corixa), a further example of burst swimming. Tilting of the oar blades would have produced lift for up, down, and sideways manoeuvrability . Examples of living subaqueous fliers are pen­ guins, and the Humpback Whale (Megaptera) . Over the years, plesiosaurs have been visualized as either rowers or fliers, but recently, closer comparison has been made with the swimming of sea-lions. These animals generate thrust partly as lift when the flip­ per is moved downwards from a horizontally out­ stretched position at the start of the propulsive stroke, and partly as drag when it is then swept backwards to lie alongside the body at the end of the stroke . Recovery is passive and feathered, but some upward lift can be produced if required . =

4 Palaeoecology

322 A

In sea-lions, the pelvic limbs are used solely for manoeuvring, but in plesiosaurs with similar sized pectoral and pelvic limbs, propulsion was probably achieved by both pairs of limbs, working out of phase to produce continuous motion (Fig. 3A) (Frey and Riess in Rayner & Wootton 1991) .

Conclusions Biomechanics is a powerful tool in palaeontology, if used with care . The paucity of palaeobiomechanical studies to date may simply reflect a lack of appreci­ ation of its possible applications, but as the studies reviewed here indicate, it has considerable potential for refining our interpretations of the palaeobiology of extinct animals .

d

References

Fig. 3 A, Swimming mode of plesiosaur; right pelvic flipper on downward part of propulsive stroke, hydrofoil section gives lift (L) in forward direction; left pelvic flipper on backward thrust (drag) part of propulsive stroke; pectoral flippers on passive recovery stroke. B, The eurypterid Baltoeurypterus rowing, shown with oar blades half-way through propulsive stroke; D, d, and V, v are drag and velocity of body and limbs respectively.

Alexander, R.McN . 1983. Animal mechanics, 2nd edn. Blackwell Scientific Publications, Oxford. McMahon, T.A. & Bonner, J.T. 1983. On size and life. Scientific American, New York. Rayner, J.M.V. & Wootton, R.J. (eds) 1991 . Biomechanics in evolution . Society for Experimental Biology, Seminar Series. Cambridge University Press, Cambridge . Selden, P.A. 1984. Autecology of Silurian eurypterids. In: M.G. Bassett & J.D. Lawson (eds) Autecology of Silurian organisms. Special Papers in Palaeontology No. 32, pp . 39- 54. Wainwright, S.A., Biggs, W.D., Currey, J.D. & Gosline, J.M. 1976. Mechanical design in organisms. Edward Arnold, London.

4.4 Hydrodynamics M . L a B A RB E R A

Introduction The field of fluid mechanics is classically divided into two subdisciplines : hydrostatics and hydro­ dynamics . Hydrostatics is concerned with the pres­ sures and pressure variation within a fluid at rest, and the pressures exerted on immersed solid bodies . Hydrodynamics encompasses a much broader di­ versity of phenomena - the forces and flow patterns that result from relative motion between a fluid and

either a solid object or another fluid . Although hydrostatics is central to some aspects of geophysics (e .g. the concept of isostasy), its application to palaeontological problems has been largely limited to studies on shelled cephalopods, where it has illuminated the mechanisms of septal chamber emptying and (with empirical data and theory de­ rived from solid mechanics) helped in estimating maximum depths for living or fossil forms .

4 . 4 Hydrodynamics Fundamentals Two properties of a fluid are central to hydrodyn­ amics, the fluid's density (p) and its dynamic viscosity ( !!), a variable that relates the rate of shear in the fluid to the shear forces :

F = S !! 8It,

(1)

where F is the shear force, S is the area parallel to the direction of shear, and 81t is the rate of shear. Another variable, the kinematic viscosity (v), is com­ monly referred to in the literature . Kinematic vis­ cosity is merely the ratio of the dynamic viscosity to the density (v = !!/p), a ratio (or its inverse) common in formulas of fluid dynamics . All references to 'viscosity' in the following discussion refer to dy­ namic viscosity. Note that both density and vis­ cosity are functions of the temperature of the fluid, and that viscosity in particular is extremely sensitive to temperature; in experimental work it is vital that the fluid be at the relevant temperature or that appropriate corrections be made . A basic assumption of fluid dynamics is the so­ called 'no slip condition', i . e . the fluid in immediate contact with any solid surface does not move with respect to the solid . Despite its counterintuitive nature, the no slip condition enjoys considerable experimental support and appears to be valid down to spatial scales of the order of the mean free path of the molecules in the fluid; the utility of this as­ sumption lies in the fact that it implies that all shear is developed within the body of the fluid, allowing direct application of equation (1) or an often more convenient formulation: 't = !!dUldl,

(2)

where 't is the shear stress and d Uldl is the velocity

gradient .

The conservation laws (mass, energy, momentum) of physics have their analogues in fluid mechanics, and proper application of these laws can simplify many experimental investigations (VogeI 1981) . The conservation of energy relation in fluid mechanics, known as the Bernoulli equation, is of particular importance, since many suspension feeding animals apparently exploit it: 2 (3) 1/2 p U + P + pgh = a constant, where U is velocity, P is pressure, g is acceleration due to gravity, and h is height above some baseline . This relationship must be used with some caution because it assumes that viscosity does not exist. Equation (3) should not be used across streamlines,

323

in regions of high shear, or for two widely separated points in the fluid, but generally gives robust qualitative predictions of the pressure differences between two points in a moving fluid .

Forces in flows In fluid mechanics, it is irrelevant if an object moves through a stationary fluid or a fluid moves past a stationary object - the flow patterns and forces in virtually all cases are equivalent. Three major kinds of forces act (Fig . 1 ) : (1) drag, a force parallel to the direction of motion which transfers momentum be­ tween the object and the fluid; (2) lift, a force acting perpendicular to the direction of motion (not neces­ sarily upwards); and (3) acceleration forces, which act whenever the relative motion of the object and fluid changes (acceleration or deceleration) . Forces in fluid dynamics may ultimately be traced to two sources : shear forces arise from the viscosity of the fluid, while pressure forces arise from the fluid's density (although viscosity may be indirectly important in modifying flow patterns, thus chang­ ing the magnitude of the pressure forces) . A con­ venient index to the relative importance of these two forces is the Reynolds number (Re) : Re = p ULl!!

(4)

where U is velocity and L is some characteristic length of the object (usually the maximum dimen­ sion parallel to the flow) . Re is a dimensionless index that can be viewed as the ratio of the inertial (pressure) forces to the viscous forces; it is central to all experimental modelling work, since equality of Reynolds numbers for a given shape implies iden­ tical flow patterns and equality of force coefficients (see below) . Any object moving at a uniform velocity with respect to a fluid experiences a drag force opposing its motion. At any Reynolds number, one source of drag is the shear of the fluid past the object; the magnitude of this drag is given by equations (1) and (2) . Note that shear always implies a drag force; even the substrate and objects lying flush with the substrate experience a drag force . At low Reynolds numbers (Re < 1), almost all of the drag force arises from viscosity; drag on planktic and small benthic organisms is thus directly proportional to the wetted surface area of the organism and to the velocity of flow. A number of useful low Re drag formulas are given by Vogel (1981) . At high Reynolds numbers (Re > 500) forces arising from the pressure differ­ ential between the front and rear of the object are

4 Palaeoecology

324 d U/dt

U

•

..

•

A D

•

A summary of the forces on an object immersed in a moving fluid. U mainstream current velocity vector; d U/dt acceleration of the object relative to the fluid, D drag force on the object, L lift force (shown acting downward to emphasize that lift need not act counter to gravity), and A force arising from the acceleration reaction . If the relative speed of the object and fluid is constant, both d U/dt and A disappear. Fig. 1

=

=

=

=

=

area, although other definitions could be used if appropriate for the problem at hand . Whenever an object accelerates or decelerates in a fluid, an additional force arises from the necessary acceleration of a volume of fluid in the opposite direction. This results in an increased effective mass of the object; the phenomenon is often referred to as the acceleration reaction . The magnitude of this force is given by: Fa

=

(1 + <x) p V dU/dt

(7)

where <X is the added mass coefficient (a dimen­ sionless shape factor), V is the organism's volume, and d U/dt is the acceleration. Forces due to acceler­ ation may either add to or subtract from drag forces; in general, the acceleration forces act to oppose changes in the relative speed of the object and fluid. For more information and a biological context, see Denny et al . (1985) .

the primary contributors to drag. In general,

D

=

!CdPS U2

(5)

where D is the drag force and Cd is the coefficient of drag. The coefficient of drag is an empirical factor relating the shape of the object to the magnitude of drag. Note that Cd must be determined for each different shape and is valid over only a limited range of Reynolds numbers (see Vogel 1981). The definition of S in equation (5) depends on the context. In the engineering literature, S is usually the frontal area for bluff bodies (spheres, cylinders, etc . ), the total surface area for streamlined bodies, the planform area for lifting bodies, or the two­ thirds power of volume (dimensionally equivalent to an area) for airships . The last definition is be­ coming increasingly common in the biological literature since it scales drag to the volume of the organism. References in the biological and palae­ ontological literature often ignore these differing definitions of the relevant area and it is important to check carefully the definition used before experi­ mental Cd values are compared to literature values . Also note that, despite many assertions in the litera­ ture, drag is proportional to velocity squared only at high Re . At high Re, appropriate shapes may generate forces perpendicular to the flow (lift) . The magni­ tude of the lift force is given by:

L

=

!Cl P S U2

(6)

where L is the lift force and Cl is the coefficient of lift. In equation (6), S is almost invariably the planform

Experimental techniques Except in the simplest cases, investigations into the hydrodynamics of fossils or sediments will involve some form of modelling. Such an approach is par­ ticularly attractive because it allows easy deter­ mination of the hydrodynamic significance of morphological features by modification of otherwise identical models . Relative motion between the model and the fluid may be produced using a towing tank, wind tunnel, or flow tank (flume); appropriate designs may be found in Vogel (1981) and Nowell & Jumars (1987) . Information and references on techniques for mapping flow patterns, measuring flow velocities, and measuring flow­ generated forces can be found in Vogel (1981 ) . Methods for making models o f fossils are strongly dependent on the specimens and available ma­ terials; no prescription is possible and investigators must depend on their own ingenuity. Models may be freely enlarged or reduced in size for experimen­ tal convenience as long as the Reynolds number is held constant. However, since identity of Reynolds num­ bers only guarantees that the force coefficients Cd and Cl (not the absolute forces) are identical, situ­ ations in which deformation of the specimen by hydrodynamic forces is an important consideration should preferably be modelled life size in the orig­ inal fluid medium. (Such situations will generally pose considerable problems in the choice of model­ ling materials and should be avoided if possible . )

325

4 . 4 Hydrodynamics A

Applications Studies of the hydrodynamics of living organisms that are potentially applicable to palaeontology are numerous and diverse; see Vogel (1981) for an introduction to the neontological literature . Palaeontological fluid dynamic studies are more limited in number, but are becoming increasingly common . In the terrestrial environment, most work has focused on the aerodynamics of flying reptiles (e . g . Brower 1983) and the evolution of flight in birds and insects (Section 1 .9); such studies have helped to clarify the significance of particular mor­ phological features and the evolutionary pathways to aerial locomotion. Niklas' (1985) work on wind pollination in living and fossil plants is a particularly instructive example of the power of fluid mechanical analysis in palaeontological and evolutionary studies . In the aquatic environment, the diversity of studies involving hydrodynamics is much greater. Locomotion tends to be the focus for much of the work, ranging from studies on molluscs (e . g . Chamberlain 1981) t o arthropods (see Section 4.3), fish (Belles-Isles 1987), and reptiles (e . g . Godfrey 1984; Taylor 1987) . Most such studies have used energetic arguments based on drag forces to explain evolutionary patterns; none has considered the possible importance of the acceleration reaction. A few studies have focused on the interactions be­ tween benthic animals, the sediment, and the hy­ drodynamic environment (e.g. Alexander 1984) . The possible use of pressure differences implied by the Bernoulli equation to create or augment feeding currents has been studied in archaeocyathids and stromatoporoids (see Boyajian & LaBarbera 1987), and feeding currents have been reconstructed for fossil bryozoans (Fig. 2) . Recently, several studies have attempted to relate the evolutionary history of particular groups to their hydrodynamics (e . g . McKinney 1986 and other references i n that volume) . One attraction of hydrodynamic studies in palae­ ontology arises from the fact that the primary factors governing hydrodynamic relations - the external shape of the organism and the Reynolds number can be determined relatively easily or estimated to a reasonable level of precision. The basic technology involved in experimental studies of organismal hydrodynamics is inexpensive, and the physical principles underlying such studies can be expected to be robust through geological time . However, as is the case in most of palaeobiology, some familiarity

B

' 8 30 20 10

-u

'"

N -u (l)

�

-u ::l

E

c (l)

;:

(l) CL

4

B

12 16

Whorl n u mber

Fig. 2 A, Flow patterns o f living Bugula turrita . B, Distribution of mud-filled zooids as a function of whorl number in fossil Archimedes intermedius . The line plotted in B is the moving average of five whorls for four nearly complete colonies . An interior stagnant region is prominant in living colonies of Bugula, and living polypides (dark squares) are largely restricted to the peripheral regions of the branches . Mud-filled zooids i n A. intermedius are presumed t o represent zooids abandoned during the life of the colony because they lay in regions of minimal water exchange . (After McKinney et al. 1986 .)

with living descendants or analogues of the fossils is vital if mistakes are to be avoided .

References Alexander, R.R. 1984. Comparative hydrodynamic stability of brachiopod shells on current-scoured arenaceous substrates. Lethaia 17, 17-32. Belles-Isles, M . 1987. La nage et l'hydrodynamique de deux Agnathes du Paleozoique : Alaspis macrotuberculata et Pteraspis rostrata. Neues Jahrbuch for Geologie und Paliiontologie, Abhandlungen 175, 347- 376. Boyajian, G . E . & LaBarbera, M. 1987. Biomechanical analysis of passive flow of stromatoporoids - morphologic, paleo­ ecologic, and systematic implications. Lethaia 20, 223 -229 . Brower, J . c . 1983. The aerodynamics of Pteranodon and Nyctosaurus, two large pterosaurs from the Upper Cretaceous of Kansas. Journal of Vertebrate Paleontology 3, 84 - 124.

326

4 Palaeoecology

Chamberlain, J.A., Jr. 198 1 . Hydromechanical design of fossil cephalopods. In: M.R. House & J.R. Senior (eds) The Ammonoitiea, pp. 289-336. Systematics Association Special Volume 18. Academic Press, London. Denny, M. W., Daniel, T.L. & Koehl, M.A.R. 1985. Mechanical limits to size in wave-swept organisms . Ecological Mono­ graphs 55, 69 - 1 02. Godfrey, S.J. 1984. Plesiosaur subaqueous locomotion: a re­ appraisal. Neues Jahrbuch fUr Geologie und Paliiontologie, Monatshefte 1984, 661 - 672. McKinney, F.K. 1986. Historical record of erect bryozoan growth forms. Proceedings of the Royal Society of London 8228, 133 - 149 .

McKinney, F . K . , Listokin, M.R.A. & Phifer, C.D. 1986. Flow and polypide distribution in the cheilostome Bugula and their inference in Archimedes. Lethaia 19, 81 - 93 . Niklas, K . J . 1985. The aerodynamics o f wind pollination. Botanical Review 51 , 328- 386. Nowell, A.R.M. & Jumars, P.A. 1987. Flumes: theoretical and experimental considerations for simulation of benthic environments. Oceanography and Marine Biology 2 5, 91 - 1 12. Taylor, M.A. 1987. A reinterpretation of ichthyosaur swim­ ming and buoyancy. Palaeontology 30, 531 - 535 . Vogel, S. 1981 . Life in moving fluids . Princeton University Press, Princeton.

4 . 5 Populations C . B . CURRY

Populations are groups o f individuals from the same species which occupy a discrete geographical region. This apparently straightforward definition masks considerable complexity, especially in rec­ ognizing fossil populations that are subject to selec­ tive preservation and post mortem transportation. In some cases it has even proved difficult to apply this definition meaningfully to living organisms because the boundaries between adjacent populations are often fuzzy or even overlapping. Furthermore, the distribution of individuals within extant popu­ lations can be far from homogeneous, and mobile organisms which migrate from one population to another (or plants with wind- or animal-transported seeds) are a further complication. The heterogeneity of population structure has led ecologists to estab­ lish a hierarchical subdivision of populations into several demes (or local populations), each of which is composed of a variable number of family groups . Such subdivisions are also difficult to apply to fossil populations, although there has been con­ siderable progress in the use of computer recon­ structions to investigate the structure of fossil populations . Computer studies (see also Section 6 . 1 ) are particularly helpful because population structure and dynamics are determined by the inter­ play of a large number of factors, the significance of which could be unravelled from computer simu­ lations . From this type of analysis it became clear

that the structure of a population, as determined from size - frequency histograms, is primarily governed by the interplay between mortality rate and growth rate, although factors such as recruit­ ment strategy and seasonal cessation of growth are also important (Craig & Oertel 1966) . A major constraint for fossil populations is the difficulty of collecting a representative sample, which some authorities argue should number at least 1000 indi­ viduals (see discussion in Craig & Oertel 1966) . In particular, many fossil populations lack juveniles, which are relatively fragile and hence much more susceptible to destruction and transportation . Arguably the most important development in population studies during the last 20 years has been the advent of genetic analyses (Mayr 1970; Wright 1978; Hartl 1980; Ayala 1982) . Such analyses are not possible for fossil populations at the present time (although new discoveries in molecular palaeon­ tology may at some future date allow the utilization of fossil molecular data in population studies, at least at a crude level; Section 2 . 1 ) . Nevertheless, the results of population genetics studies are of direct relevance for palaeontologists because they are beginning to reveal the fundamental features of populations and of their spatial and temporal behaviour. The recent technological advances in genetics have provided a series of powerful new research

327

4 . 5 Populations tools which can investigate the prodigious infor­ mation stored in DNA, RNA, and proteins . Using such techniques it is possible to measure accurately molecular variability both between individuals of a single population and between different popu­ lations of a single species. The ability to quantify intra- and interpopulation variability is certainly a major step forward, and such data can be used to investigate how populations develop and evolve . Geneticists define populations as communities of individuals which are linked by bonds of mating and parenthood, and hence share a common gene pool. This definition applies only to sexually re­ producing populations, which are also known as Mendelian populations to distinguish them from those populations that are united by parenthood and a common gene pool but which reproduce asexually. Population genetics has become an active and often hotly debated branch of genetics . Measurements of the extent of genetic variation between individuals of a population, known as genetic distances, allows the precise description of populations on the basis of their total genetic varia­ bility; this can be investigated over several gener­ ations, or directly contrasted with that of other populations, to provide information on population structure and dynamics. Population genetics is an inherently mathematical subject which can become very complex, both in terms of how genetic distances are calculated and how the resulting data are com­ piled, presented, and interpreted (Nei 1972; Nevo 1978) . The most precise (and hence most desirable) method of quantifying genetic variability is to deter­ mine the sequence of nucleotide bases in homolo­ gous regions of DNA or RNA. But direct sequencing is complex and extremely time-consuming, and was rarely a practical option at the time when interest in the genetics of populations was developing . Instead, population geneticists made use of several other techniques which yielded quick results and pro­ vided less accurate but still extremely useful esti­ mates of genetic variability within individuals and populations . By far the most widely used method of estimating genetic variability is gel electrophoresis of enzymes . This effectively detects DNA variability a t 'second­ hand', because enzymes are functional proteins pro­ duced from the coded information stored in DNA sequences. Individuals can contain one or more vari­ ants of a single enzyme, each of which is produced by different versions of a single gene (alleles) which have distinct nucleotide sequences . The dis-

covery that variants of a single enzyme, known as aUozymes, could be distinguished using gel elec­ trophoresis therefore provided geneticists with a convenient method of estimating genetic variability relatively quickly and with reasonable accuracy. Gel electrophoresis makes use of the different prop­ erties of allozymes in a direct electric field - both their direction and rate of migration varies accord­ ing to their net electric charge and molecular size . Thus allozymes show up as discrete bands when subjected to gel electrophoresis (Fig . 1 ) . To achieve a reasonable estimate of genetic variability, it is important that a sufficient number of randomly­ chosen enzymes are investigated, and that a suf­ ficiently large sample of individuals is measured from each population. From the pattern of enzyme variability, as re­ vealed by bands in gel electrophoresis, each indi­ vidual can be described as homozygous (with only one allozyme) or heterozygous (two or more allo­ zymes) for that particular coding gene locus (Fig. 1 ) . The overall genetic variability o f the population can then be expressed in terms of the number of polymorphic (i. e . heterozygous) loci (Table 1 ) . In an attempt to standardize measurements of population polymorphism, geneticists had to decide on an arbi­ trary criterion to distinguish between polymorphic and non-polymorphic loci . Polymorphic loci are generally defined as those for which the dominant allele has a frequency of not more than 0 . 95 . Thus in surveying 100 individuals from a single population for allozyme A or allozyme B, the gene locus coding for this particular enzyme would be considered polymorphic if 95 organisms had A and five had B, but it would be considered non-polymorphic if

- - -

e

-

-

- - -

-

-

-

-

-

-

-

- - - - - - - - - -

1

2

3

4

5

6

7

8

9

10

Samples

Fig. 1 Gel electrophoresis of allozymes determined for ten individuals. After separation in an electric current, speci­ mens 1, 2, 4, 6, 8, 9, and 10 are seen to be homozygotes for this particular enzyme (i. e . only one band), while the rest are heterozygous (more than one band) .

328 Table 1

4 Palaeoecology Genetic variability in different groups .

Organism

Number of species

Loci studied

Polymorphism (%)

Heterozygosity (%)

17 14 28 6 4 5 14 11 9 4 30

16 23 24 15 18 18 21 22 21 19 28

26 .4 43.9 52. 9 24. 3 53. 1 43 . 7 30. 6 33 . 6 23 . 1 14.5 20 . 6

4.6 12.4 15.0 6.2 15.1 5.0 7.8 8.2 4.7 4.2 5.1

Plants Marine invertebrates Flies Wasps Insects Land snails Fish Amphibians Reptiles Birds Mammals

96 individuals had A and only four had B . The overall genetic variability of the population can therefore be expressed as the proportion of poly­ morphic loci (Table 2), or simply Polymorphism (P) . Polymorphism is, however, an imprecise measure of genetic variation because it does not distinguish between loci which are only slightly polymorphic (for example with two or three alleles) and those which display extreme variability (e . g . with 20 or more alleles) . Consequently, polymorphism alone is not considered a very useful measure of genetic variability, although it is often cited in the literature . A more widely used measure of population varia­ bility is heterozygosity (H), which is much more precise and does not depend on arbitrary determi­ nation of polymorphism. The heterozygosity of a population is measured by first determining the frequency of heterozygous individuals at each locus, and then averaging these frequencies over all loci (Table 3) . Such de terminations are limited by the ability of gel electrophoresis to detect mobility variations between allozymes, and almost certainly underestimates the total genetic variability present because allozymes with relatively similar net electric charge will not be resolved . In addition, allozyme Table 2

studies d o not provide any information o n the ex­ tent of nucleotide substitutions in non-coding re­ gions of DNA (the introns, which can represent very large proportions of the genome), and hence electro­ phoresis is known to underestimate genetic vari­ ation at the enzyme level by an unknown amount. Despite these problems, allozyme electrophoresis was rapidly adopted as the standard method for investigating population genetics, and many thou­ sands of studies have been carried out since the technique was first described in 1966. Recent tech­ nological advances have now made it practicable to measure DNA variability directly, but such methods have not yet been as extensively applied, and the allozyme data remains unsurpassed in providing directly comparable population data on representa­ tives of all the major life forms . The major surprise from allozyme studies was the discovery that there is much more genetic varia­ bility in individuals and populations than had pre­ viously been suspected . In general, invertebrate animals have much more genetic variability than vertebrates, with the average heterozygosity among invertebrates being more than double that of the vertebrates (Table 1). Even the lower heterozygosity

Calculation of average polymorphism in five populations. Number of loci Population 1 2 3 4 5

Polymorphic

Total

19 15 14 18 17

30 30 30 30 30

Polymorphism (P) % 63 50 47 60 57

Average

=

55.4

4 . 5 Populations Table 3

329

Calculation of average heterozygosity at ten loci. Number of individuals Locus 1 2 3 4 5 6 7 8 9 10

Heterozygotes

Total

56 16 28 0 8 41 6 21 3 12

100 100 100 100 100 100 100 100 100 100

levels represent an enormous amount of variability, considerably more than is needed to ensure that, with the exception of identical twins, all human beings, past, present, and future, will be genetically distinct . The vast amount of genetic data now ac­ cumulated demonstrates that the average interpopu­ lation genetic distances are consistently smaller than, although overlapping with, the genetic dis­ tances between subspecies, species etc . (Fig . 2) . In simple terms, such differentiation reflects the in­ creasing degree and longevity of genetic isolation inherent in ascending the taxonomic hierarchy (White 1977; Templeton 1980) . More recently, a number of new and potentially more powerful methods of measuring genetic varia­ bility have become available . Mitochondrial DNA has particular significance for population studies because in many phyla it evolves much faster than

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the nuclear DNA in the chromosomes, and hence offers a much more precise measure of relatively recent divergence events . Direct sequencing is now possible on a routine basis, but there are still con­ siderable problems to be overcome in the interpret­ ation of such data. The recognition of mutational 'hot-spots', where the DNA is subject to rapid sub­ stitutions, perhaps many times over at the same place, means that direct sequencing may not neces­ sarily always be an ideal tool for the population geneticist, and indeed could be very misleading. The importance of population genetics stems from the fact that populations are seen as fundamental units of evolution. The genotype (the total genetic content) of an individual is fixed from birth, but the overall population gene pool is dynamic and can change from generation to generation, thereby providing the variability on which evolutionary processes act .

References

2.5 2.0 1 .5 1 .0 0.5

Po p u l a t i o n s

Sibling species

Congeneric s pe c i e s

Representation of the increasing ranges of genetic distances measured between populations, sibling species, and congeneric species. Data compiled from a large number of studies using gel electrophoresis of allozymes .

Fig. 2

Heterozygosity (H) %

Ayala, F.J. 1982. Population and evolutionary ecology: a primer. Benjamin-Cummings Publishing, Menlo Park. Craig, G . Y . & Oertel, G. 1966. Deterministic models of living and fossil populations of animals. Quarterly Journal of the Geological Society of London 122, 315-355. Hartl, D . L . 1980. Principles of population genetics . Sinaeur, Sunderland, Ma. Mayr, E . 1970. Populations, species and evolution . Harvard University Press, Cambridge, Ma. Nei, M. 1972. Genetic distance between populations . American Naturalist 106, 283 -291 . Nevo, E. 1978. Genetic variations in natural populations : pat­ tern and theory. Theoretical Population Biology 13 , 121 177. Templeton, A.R. 1980. The theory of speciation via the foun­ der principle. Genetics 94, 101 1 - 1038 .

330

4 Palaeoecology

White, M.J.D. 1977. Modes of speciation. W.H. Freeman, San Francisco. Wright, S. 1978. Evolution and the genetics of populations. 4:

Variability within and among natural populations. University of Chicago Press, Chicago.

4 . 6 Coloniality B . R . ROSEN

Introduction

Colony has been used most consistently to refer to a population of a single species whose members have grown from one another but remained physically attached to each other. It follows that coloniality refers to the habit of living in colonies . Although there are other populations that have been called colonies, such as physical overgrowths (e . g . oysters, serpulids), sessile and mobile aggregations (e . g . barnacles, ophiuroids), and separate animals that live in functional or social systems (e .g. sea-bird colonies, fish and cephalopod shoals, ungulate flocks and herds), they are excluded here . Although the above definition of coloniality is based on growth pattern, most organisms so defined are morphologically identifiable because they clearly consist of numerous similar colony members (like zooids or polyps) . Thus, bryozoans and graptoloids are generally regarded as exclusively colonial, while Hydrozoa, anthozoan corals, and tunicates include numerous colonial representatives . Sponges are enigmatic because they have no obvious and con­ sistent features that one might regard as colony members, and consequently are taken to be solitary by many workers . For a more complete phyletic survey, see Wilson (1975, p. 389) . Colonial organisms are entirely aquatic, mostly marine and sessile. Colonies are common on hard substrates, being especially important on reefs . Salps (Tunicata), siphonophores (Cnidaria), and graptoloids, however, are or were pelagic. Colonial organisms are amongst the largest and longest­ lived of all organisms . Most possess mineralized skeletons (notably cnidarians and bryozoans) and collectively are represented throughout most of the Phanerozoic . Palaeontological authors in Boardman et al. (1973) were influential in initiating much of the current

biological interest in coloniality, developing Beklemishev's ideas about integration in inver­ tebrate colonies (see below) . Ironically, however, palaeontologists cannot really answer many of the key questions from the study of fossils alone, and it is inevitable that the emphasis in coloniality studies has since become neobiological . This is clear from the contents of all the more recent multiauthor vol­ umes in this field (Larwood & Rosen 1979; Jackson et al. 1985; Harper 1986; Harper et al . 1986) . Even more ironically perhaps, the most important sub­ sequent influence in this subject has come from outside zoology altogether, from what may seem the surprising source of plant population ecology (Harper 1977) . For palaeontologists, the greatest scope for studying coloniality lies in investigations of patterns of form through time, form in differ­ ent palaeoenvironments, and inferences of colony growth patterns (astogeny) from fossil collections at different growth stages .

Clonal growth and form Two aspects of growth and form, clonoteny and iteration respectively, provide the most precise framework to date for discussing and investigat­ ing colonies (Table 1) (and also permit sponges to be considered colonial in particular instances) . Clonal life histories are extremely varied . The kinds of physically continuous colonies typified by cnidarians and bryozoans have grown by the bodily retention of clonal individuals (clonoteny), though many of these same organisms can also initiate new colonies by shedding their clonal offspring (clonopary), either passively (e .g. through colony breakage and partial mortality) or as part of an in­ herited growth pattern . Clonal organisms can often fuse too, and this represents a non-clonotenous component of colony building (though it is likely

331

4 . 6 Coloniality Table 1

Criteria and terminology of coloniality.

Life history

Body plan unitary (non-iterative, non-modular, non-colonial, solitary)

Body plan iterative (consisting of iterative units or modules derived from each other by continuous growth and attached to each other) Colonies

(in the sense of having iterative form only) Aclonal offspring by sexual reproduction only -

One zygote develops into one unitary organism

One zygote develops into one iterative organism

One level of physical individuality

Two levels of physical individuality: Iterative units, e . g. zooids 2 Colonies 1

e.g. humans (except identical twins)

e.g. most trees, graptoloids, siphonophores and (by default) all iterative organisms without known clonal habit Colonies

(in the sense of being c/onotenous, hence iterative in form) Clonal offspring by sexual reproduction and cloning -

All clones shed (clonopary, iteropary, fission) by parent

Some clones shed (clonopary, iteropary, fission) and some retained (clonoteny) by parent

One zygote develops into one clonal lineage (genet) of numerous genetically identical unitary ramets

One zygote develops into one clonal lineage (genet) of numerous genetically identical iterative ramets

Two levels of physical individuality: 1 Ramets 2 Genets

Three levels of physical individuality: 1 Iterative units, e . g . zooids 2 Ramets colonies 3 Genets

e.g. Amoeba, some flatworms, Hydra, many sea anemones, some solitary corals like Fungia; also aphids, water fleas and rotifers (by parthenogenesis)

e.g. many hydrozoans and octocorals, colonial corals, tapeworms, some polychaetes, some bryozoans, tunicates, salps, strawberry plants

=

Notes: (1) In practice, different authors' definitions vary slightly; (2) there is some transition between the two concepts of coloniality on the right hand side because some iterative-only organisms (upper right) are occasionally clonoparous; (3) in the case of iterative-and­ clonotenous colonies (lower right), new ramets might be unitary at the outset and become iterative, or be iterative at the outset; and (4) Modules is meant here in Harper's sense - see text.

that only members of the same infraspecific clonal strain can do this) . In bulk terms, it is not the main colony-building process . In fossils it is some­ times difficult to distinguish fusion from post mortem overgrowth . Although aggregations were excluded (above) from colonies, the members of many organisms that live in close populations or societies are also clonoparous, or have life histories in which at least some members are produced parthenogenetically (e . g . aphids) or from unfertilized eggs (e . g . male honey bees) . In this respect, populations of these organisms have been likened to colonies within

which the physical connections between members are virtual rather than real. Cloning must also be seen in the wider context of reproduction and dispersion. In many sessile clono­ parous organisms, clones may remain close to their parents, while other organisms show combinations of cloning patterns that include both clonotenous colonies as well as a clonoparously produced vagile phase (e . g . the cnidarian medusa) . Even the lar­ val phase in Cnidaria, generally zygotic in origin, can be produced clonoparously by some taxa . Thus clonal organisms can variously allocate resources to growth of existing individuals, production of clonal

4 Palaeoecology

332

offspring (which can either be shed or retained by the parent growth), or to sexual reproduction . A remarkable consequence of this is that, whereas in non-clonal organisms a single zygote generally produces a single individual, in a clonal organism it is represented by two or more physical levels of individuality, all genetically identical (Table 1 ) . The whole single-zygote population unit i s a genet, which consists of clonoparously produced units (ramets) . Ramets in different organisms can be solitary or colonial . Within colonies, units may have different forms and functions (polymorphs, as in siphonophores, many bryozoans (Fig. 1), and hydro­ zoans) . Clearly, the simple ecological concept of an individual as it applies to non-colonial organisms is inadequate for colonial organisms . Not only are there several levels of individuality to consider but also the dynamic relationships between them . The basic demographic parameters of births, deaths, immigrants, and emigrants used for non­ colonial organisms can be applied on all these levels .

On one level, a colony's growth can be studied by treating its within-colony individuals as a popu­ lation (metapopulation) and applying standard demographic concepts (e . g . number and colony lo­ cation of births and deaths of different kinds of zooids through time) . On another level, an ecological survey based on coral heads (i. e . whole colonies) uses ramets as its individual units . At both the ramet and genet level, the number of intracolonial individuals, as well as number of ramets themselves, appears to increase indefinitely through time, the main exception being organisms whose colonies have determinate growth (e . g . many pelagic forms, such as graptoloids) . While their within-colony individuals may senesce and perish, there is usually a turnover in their population, with a net increase . Colonies (ramets) themselves often show no obvious signs of senescence and the genets of many clonal organisms seem to be virtually im­ mortal . It follows that fecundity (the potential for sexual reproduction) of a clonal organism increases,

Fig. l A, Scanning electron micrograph (x 36) of the skeleton of a cheilostome bryozoan colony, Smittina exertaviculata Rogick; BM(NH) D53488, subfossil, McMurdo, Antarctica, showing polymorphic iterative units grouped into cormidia ( x 36) . (Photograph courtesy of P.D. Taylor . ) B, Key to colony organization in A. Each kind of polymorph (A,AZ,O) is seen here in its zooecial (skeletal) part only. In the living animal, each corresponds to a different kind of zooid or zooidally-derived structure . A avicularium (?defensive role) within orifice of autozooecium, AZ autozooecial frontal wall with pores (autozooid has feeding function), 0 ovicell (brood chamber), or autozooidal orifice, C cormidium. Arrow gives direction of growth (from proximal to distal). Ovicells and avicularia are not present throughout colony. Although ovicells function with respect to the adjacent proximal autozooid, they may originate from either this or the adjacent distal zooid . =

=

=

=

=

4 . 6 Coloniality generally exponentially, with the age of both ramets and genets, in distinct contrast with non-clonal organisms, whose potential (i. e . for a given zygotic individual) usually peaks and then declines . As a result of all these traits, as well as the possible occurrence of colony fusion, it is clear that the standard working concepts of population biology individuals, births, deaths, age, senescence, fec­ undity, and size - together with the relationships between them, as widely understood for non-clonal organisms, do not apply in the same way, if at all, to clonal (hence colonial) organisms .

Individuals, iteration, and modularity Although the most satisfactory concept of a colony is based on clonal features, the simplest practical way of identifying a colony is on the occurrence within it of numerous similar intracolonial individuals, like zooids (Fig. 1). This is straightforward if these individuals closely resemble a solitary counterpart. The polyps of cnidarian colonies, for example, can be compared directly with solitary cnidarians like Hydra or sea anemones . This approach encounters difficulties, however, when the supposed colony individuals do not clearly resemble known solitary counterparts . For instance, a colonial coral whose corallite walls are incomplete or absent effectively consists of a multi-mouthed (cerberoid) body sharing one coelenteric cavity. On their own, these mouths do not represent a plausible solitary organism . Are cerberoid corals 'individuals' with many mouths, or 'colonies' of mouths with one coelenteron? In the case of sponges, we do not have a recognizable body plan at all - just repeated functional features like aquiferous units, or anatomical units like cells and spicules . This problem of identifying colony individuals is also highlighted by polymorphism . The spinozooids of some bryozoans for example, differ very much from the basic bryozoan body plan. Polymorphic groups of individuals are also frequently organized in higher level intercommuni­ cating systems (cormidia) of great functional impor­ tance which are themselves repeated (Fig. 1). Do these cormidia represent the colony individuals or do the zooids? While clonoteny provides the most theoretically satisfactory criterion of coloniality, recognition of a clonal habit is not usually possible without long term observations . For fossil organisms, cloning must remain an inference . In most of the examples (above) where the criterion of identifying a clear intracolonial individual is a problem, it can be

333

circumvented by using Harper's (1977) alternative criterion of iteration (Table 1), derived largely from botany. Harper refers to all iterative features (above the cell level) as modules, though the word actually has several other older botanical meanings within his broader concept. For the sake of space and clarity here, it is more satisfactory to call them

iterative units. In practice, many living iterative organisms are also clonoparous, but the two phenomena are cer­ tainly not identical . Trees are iterative, but (horti­ cultural cuttings aside) only a few are clonoparous . Pelagic iterative organisms show only a limited capacity for clonopary: isolated zooids of physo­ nectid siphonophores, for example, cannot produce new colonies, and evidence for cloning in graptol­ oids is confined to only a few taxa . Conversely, there are many organisms (Table 1, lower left) that are clonoparous but unitary (not iterative), though this point partly depends on choice of iterative unit, since the concept of iteration is deliberately broad. The distinction between iteration and cloning is also palaeontologically useful because although coloniality-sensu-clonoteny can only be inferred in a fossil, coloniality-sensu-iteration can easily be ob­ served. The idea of iterative units, however, can lead to triviality or over-enthusiastic application . Tentacles, zooids, cormidia, o r branches i n a coelen­ terate colony might all be designated iterative units depending on relevance to a particular problem, but on many biological considerations zooids would be the primary choice .

Ecological significance Since unitary and non-clonal organisms exist and flourish as abundantly as iterative and clonal organ­ isms, it is impossible to state absolute benefits of coloniality. It appears to confer advantages for par­ ticular organisms in particular environments (e . g . corals o n reefs) . Most ecological scenarios concern­ ing coloniality originate from size considerations . Assuming that every organism has mechanical constraints on the ultimate size of its body plan, mainly arising from changing ratios of surface area : volume, then one (but not the only) escape from these constraints is iteration . Presumably iteration developed in those (mostly lower) organisms that already possessed the ability to clone or to regener­ ate . Their consequent ability to grow very large seems to have enabled them to occupy substrate or the space above it, or both, more effectively than their unitary counterparts . It also improved their chances

334

4 Palaeoecology

of surviving adverse events . Diversity of colony form can be interpreted as different ways of obtain­ ing resources and of responding to otherwise un­ favourable circumstances like heavy wave action, muddy substrates, and intense grazing . For the large number of colonial organisms that are also fixed to the substrate, iteration provides a form of mobile behaviour . Although adverse con­ ditions may kill off parts of a colony, other parts survive and, in effect, escape . Storms, and sud­ den increases in wave and current action dam­ age whole stands of iterative organisms, but their broken pieces are often swept into sheltered places and survive . Ramets and iterative units are often destroyed, yet the genotype survives . Another behavioural consequence o f iteration is the ability to grow in a particular direction, or to develop more of one kind of specialized zooidal polymorph than another, in response to particular environmental events or gradients . Iterative organ­ isms characteristically show great intraspecific plas­ ticity of colony form, some of it in response to different conditions . Iteration appears to confer great flexibility on how a colonial organism fills its occupied spatial envelope . This in turn reflects the capacity of colonial organisms to vary the ecologi­ cally significant relationships between their bio­ mass, surface area, actual colony volume, and their spatial envelope (though not necessarily within a single colony or taxon) . Phalanx growths (sheets and mounds) can blanket a substrate to the exclusion of other benthos, and take maximum advantage of locally favourable conditions, whereas guerilla growths (runners, often branching or anastomosing) can occupy a broader spatial envelope on a given substrate much more quickly, circumvent hostile neighbours, and rapidly find the most suitable sites (spatial refuges) in very patchy microenvironments (see also Section 4.9) . The ability of some iterative organisms to grow much further away from their substrate than a single body plan allows, even from a small densely­ occupied area, gives access to better or different con­ ditions from those closer to the substrate (e . g . food bearing currents, clearer water) . Typical of such forms are mounds, plates, and especially branching forms like trees . Tree-like forms share some of the features of guerillas in three dimensions, because they can forage, explore, or circumvent habitat fea­ tures . Although branching is one of the most com­ mon modes of clonotenous colony increase (e . g . corallites in rugose corals), i t also arises a t higher organizational levels, as in the zooidal groups

that make up the branches of ramose tabulate and scleractinian corals . Growth and plasticity in iterative organisms can be explored in terms of three parameters: 1 An inherited growth plan (architectural model) which is topologically constant (i. e . always has the same definitive qualitative growth plan) . To judge from tropical trees, there is only a surprisingly small number of realized models (Halle et al. 1978) . 2 Quantitative modifications to this pattern (e . g . branching angle), which may b e phenotypic o r en­ vironmentally induced, or both . 3 Reiteration of the whole architectural model (e . g . i n response t o a traumatic event) . Pelagic iterative organisms like siphonophores, salps, and graptoloids differ in many respects from sessile iterative organisms, especially in their re­ duced plasticity and clonopary, and in having de­ terminate growth form . Nevertheless, iteration can again be interpreted in terms of size, with enhanced resource capture, more effective swimming and floating, and better chances of surviving predatory attack compared with unitary forms .

Functional significance Iteration is usually associated with various levels of integration between units . This commonly in­ cludes sharing of resources, intercommunication for defensive retraction of zooids, co-operation in capturing and consuming resources (including prey that are much larger than the iterative units), and maintenance of colony form following damage . Un­ fortunately, because these dynamic aspects of inte­ gration are not observable in fossils, they can only be inferred - mainly on indirect skeletal evidence such as presence of interconnecting structures be­ tween zooids and loss of morphological distinct­ ness ('identity') of zooids . Nevertheless, W.N. Beklemishev's idea (further developed by Boardman et al . 1973) that integration becomes more complete as colonial organisms evolve has been a great influence and has so far proved to be a reasonable hypothesis, even on these skeletal grounds alone (but see Mackie in Harper et al . 1986) . A related widespread feature of colonial organ­ isms, best seen in hydrozoans, siphonophores, and bryozoans, is the division of functions between their polymorphic iterative units (e . g . reproduction, prey capture, larval brooding, swimming, and main­ tenance of colony-wide feeding currents), analogous to the role of organs in a unitary animal (Fig. 1 ) .

4 . 6 Coloniality So complete is this organizational and functional integration in some organisms that authors have referred to them as 'superorganisms' .

Evolutionary significance The ability of colonial-sensu-clonal organisms to exist as numerous separate ramets within a single genotype, and for their genets to grow indefinitely in space and time, represents a highly developed alternative to : (1) sexual reproduction for initiating new individuals, albeit of the same genotype; and (2) the customarily cited advantages of genetic heterogeneity (i . e . as derived from sexual repro­ duction) . On the other hand, the vast numbers of sexually mature iterative units present within a single genet at any one time suggests that these organisms have retained this as an important op­ tion. So far, however, these observations have not so much generated satisfying explanations as cast doubts on the validity of current textbook general­ izations about populations, genetics, dispersion, selection, and evolution, since these are almost en­ tirely based on unitary, non-clonal organisms . One idea is that if potential habitats for colon­ ization are not environmentally heterogeneous or unstable, there is no clear benefit in having geneti­ cally diverse progeny. As large numbers of iterative units within sessile colonial organisms are often also fertile, however, high fecundity seems to of­ fer an alternative in the event of a significant en­ vironmental disturbance . This would be important for those species (such as reef corals) whose main vagile phase is a sexually produced larva . It may be that genetic turnover, and hence evolutionary rates, should be slower in clonal compared with aclonal organisms, but Jackson and Coates' comparison (in Harper et al. 1986) of their respective geological longevities has revealed no clear difference . One reason for this similarity may be that, although it is reasonable to assume that ramets within a single genet are genetically identical, a genet overall can be so long-lived that genetic variants (and hence evolutionary novelties) could conceivably arise even without sexual reproduction,

335

appearing gradually within the ramet-lineage of a single genet (i . e . mitotically) . An additional rel­ evant factor that increases this possibility is that, whereas in unitary organisms gametogenesis is localized within a single body, and is under cen­ tral control (genetically and physiologically) within that body, gametogenesis in clonal organisms con­ tinues indefinitely in time and space without any evident central control (i . e . between ramets of a single genet) . Suppose any such spontaneous gen­ etic variants were also subject to environmental selection, and were even to find their way into gametes and so be passed on to other generations of genets? Clonal organisms have yet to be properly incor­ porated in models of evolution by natural selection (van Valen 1987) . It seems that, for at least some col­ onial organisms, even the possibility of Lamarckian factors in their evolution cannot be ruled out .

References Boardman, R.S., Cheetham, A.H. & Oliver, W.A., Jr (eds) 1973. Animal colonies: development and function through time. Dowden, Hutchinson & Ross, Stroudsburg. Halle, F . , Oldeman, R.A. & Tomlinson, P.B. 1978 . Tropical trees and forests: an architectural analysis . Springer-Verlag, Berlin. Harper, J. L . 1977. Population biology of plants . Academic Press, London. Harper, J.L. (ed . ) 1986. Modular organisms: case studies of growth and form . Proceedings of the Royal Society of London B 228 , 109 - 224. Harper, J . L . , Rosen, B.R. & White, J. (eds) 1986 . The grmvth

and form of modular organisms . Proceedings of a Royal Society Discussion Meeting held on 27 and 28 June 1 985. The Royal Society, London. (First published in Philosophical Transactions of the Royal Society of London B313, 1 -250. ) Jackson, J . B . C . , Buss, L.W. & Cook, R.E. (eds) 1985 . Population biology and evolution of clonal organisms . Yale University Press, New Haven. Larwood, C . P . & Rosen, B.R. (eds) 1979 . Biology and system­ atics of colonial organisms. Systematics Association Special Volume 1 1 . Academic Press, London. van Valen, L.M. 1987. Non-Weismannian evolution. Evo­ lutionary Theory 8, 101 - 107. Wilson, E . O . 1975. Sociobiology: the new synthesis . The Belknap Press of Harvard University Press, Cambridge, Ma.

4 . 7 Stromatolites S . M . AWRAMIK

deposits . Today, stromatolites, although rare, are forming in a wide variety of marine and non-marine environments that include shallow subtidal (normal marine to hypersaline waters) to supratidal settings, lakes, streams, and thermal springs . Stromatolites provide a variety of environmental and ecological evidence, as follows : (1) their pres­ ence indicates the activity of photosynthetic mi­ crobes . For the Early Archaean, stromatolites are important indicators of the presence of microbio­ logically complex life; (2) they indicate deposition

Introduction Stromatolites are organosedimentary structures produced by the sediment trapping, binding, and! or precipitation activity of photosynthetic micro­ organisms, principally cyanobacteria (blue-green algae) . Most fossil stromatolites are found preserved as limestone or dolostone in the form of laminated domical and columnar structures, centimetres to metres in size . Other types of constructions are also grouped with stromatolites : (1) planar to wavy lami­ nated stratiform structures, the so-called cryptal­ galaminites; (2) unlaminated to poorly laminated loaf- to mound-shaped structures with a macro­ scopic clotted fabric, called thrombolites; (3) globu­ lar, unattached structures called oncolites that have incompletely enveloping laminae; and (4) Recent unlithified microbially accreted sedimentary struc­ tures of various geometries, termed microbial mats or algal mats . Occasionally, ancient stromatolites, composed partially or entirely of chert, are found to contain fossilized microbes that commonly resemble cyanobacteria (Figs 1, 2) . Fossilized prokaryotes and stromatolites are the oldest fossils known on Earth (see Section 1 .2) . Se­ quences c. 3500 Ma in Western Australia and South Africa have yielded surprisingly well developed stromatolites . However, stromatolites are rare in the Archaean (3800-2500 Ma), with less than 20 oc­ currences known . During the Proterozoic (2500c. 570 Ma), stromatolites became very abundant and diverse . They are the most conspicuous fossils dis­ covered from this eon. Several Proterozoic colum­ nar stromatolites are morphologically distinctive enough to merit taxonomic description, and some appear to have restricted time ranges (Section 2 . 1 3 . 1 ) . Stromatolites waned in diversity and abun­ dance during the transition into the Phanerozoic and became comparatively minor marine fossils for the remainder of geological time . During the Late Cambrian and Early Ordovician, they underwent a slight resurgence and became locally abundant. Although most stromatolites are from marine or pre­ sumed marine sequences, non-marine stromatolites are found in strata as old as Late Archaean . Stroma­ tolites are rather common in Cenozoic non-marine

Silicified columnar-branching stromatolite from the 2000 Ma, Gunflint Iron Formation, Canada, x 1 . 1 .

Fig. 1

c.

Fig. 2 Photomicrograph of filamentous and coccoidal cyanobacterial microfossils in Gunflint stromatolite from Fig. 1, x 380 .

336

4 . 7 Stromatolites under permanently or intermittantly aqueous con­ ditions; (3) they indicate deposition in shallow environments, within the photic zone . Unfortunately, without diagnostic sedimentary structures, stro­ matolites cannot provide a more precise indicator of permanently submerged or periodically exposed settings; (4) the presence and direction of currents can be determined by the shapes of domical and columnar stromatolites . They commonly elongate and oversteepen toward the direction of sediment supply or current (Fig. 3); (5) oncolites are useful indicators of agitation in marine settings; and (6) some Proterozoic and a few Cambrian stromatolites (in particular, columnar, columnar-branching, and conical stromatolites) are useful in biostratigraphy.

337

Modern subtidal columnar stromatolites off Lee Stocking Island, Bahamas. They are oversteepened and lean in the direction of current and sediment supply . Fig. 3

Recent stromatolites Although not abundant today, stromatolites are forming in a variety of environments (Figs 3, 4) . They are known from such non-marine settings as streams, lakes, thermal springs and even re­ frigerated environments like the frozen lakes of Antarctica. In marine environments, their distri­ bution ranges from subtidal to supratidal and from hypersaline to normal marine . Cyanobacteria are the dominant micro-organisms involved in stro­ matolite construction; however, other photosyn­ thetic microbes, including diatoms, green algae, red algae, and chloroflexacean bacteria, contribute to accretion . The micro-organisms that build stro­ matolites are organized into complex communities consisting of a few to several tens of species . A common theme among the modern occurrences of stromatolites from all environments is the sharply reduced activity of epifaunal, grazing, and bur­ rowing animals, and macro-algae and plants, caused by one or several ecological factors: elevated salinity or alkalinity, periodic desiccation, elevated temperatures, precipitation of mineral matter during growth (this creates hard, indurated sub­ strates), and strong currents or wave action . One of the major problems facing the use of Recent stroma­ tolites in the interpretation of ancient forms is that no modern analogues have yet been discovered cor­ responding to the large number of columnar and col­ umnar branching shapes found in the Proterozoic .

Ancient stromatolites Fundamental differences exist between the pre­ Phanerozoic, the Phanerozoic, and the Recent. The most significant differences with respect to stro-

.. '

.. "- ..

Fig. 4 Modern domical and columnar stromatolites from the intertidal zone of Hamelin Pool, Shark Bay, Western Australia.

matolites are as follows : (1) animals do not appear in the fossil record until � 650 Ma; (2) eukaryotes do not appear in the fossil record until c. 1500 Ma . Thus, the possible influences of algae, other protists, or even fungi on stromatolites could not have been expressed until the Middle and Late Proterozoic. There is no suggestion that these early eukaryotes directly affected stromatolites; (3) prior to 2300 Ma, the Earth was essentially anoxic . Oxygen levels were probably very low for the remainder of Early Proterozoic time . During the Middle and Late Proterozoic, oxygen levels gradually increased, so that by the latest Proterozoic (� 650 Ma, metazoan respiration could have been supported; (4) shallow marine, carbonate accumulating environments (en­ vironments where stromatolites have thrived) were

338

4 Palaeoecology

different in the pre-Phanerozoic. The dominant car­ bonate sediment was lime mud with relatively few sand-sized or coarser carbonate grains available . During the Phanerozoic, carbonate secreting in­ vertebrates and algae produced abundant coarse­ grained sediment that was readily available in agitated environments; and (5) although morpho­ logically similar to modem stromatolite builders, the microbes that built pre-Phanerozoic stromato­ lites might have been phenotypically different for some characteristics as well as genotypically differ­ ent from extant microbes .

The Archaean . Archaean stromatolites are rare; the number of localities known with convincing examples is less than 20 . The stromatolites are rela­ tively simple, exhibiting what could be termed a 'generalized' morphology . They are typically strati­ form, domical, and columnar-layered, shapes common throughout the fossil record . Columnar, columnar-branching (with simple branching pat­ terns), and conical stromatolites are rare . The com­ plex varieties known from the Proterozoic, such as complexly branching columnar stromatolites, are unknown . Environments in which Archaean stro­ matolites formed included permanently submerged to periodically exposed marine settings, as well as lacustrine to fluviatile settings . The rarity of Archaean stromatolites is probably due not to the lack of suitable microbiological constructors, but to the tectonic-sedimentary environments of green­ stone belts in which relatively stable, shallow-water, low sediment-input environments were rare . The presence of 3500 Ma, early Archaean stro­ matolites in two greenstone belts, one in Western Australia (Waiter et al . 1980) and the other in South Africa (Byerly et al . 1986), argues convincingly that microbes had already evolved the phenotypic attri­ butes necessary for stromatolite construction . Although not morphologically complex, the stro­ matolites are nevertheless well laminated and range in shape from undulatory, stratiform structures to domical structures (Fig. 5); some of the stroma to­ lites have a pseudocolumnar and columnar-layered organization, and all are morphologically very similar to Proterozoic and Phanerozoic examples . Filamen­ tous and coccoid microfossils have been discovered in chert from strata near the stromatolites in both regions (e .g. Awramik et al . 1988) . At the Western Australian site, most of the filaments occur within thinner, dark laminae of wavy laminated, light- dark laminar couplets, and they are commonly oriented parallel to the lamination - an organization that

Fig. 5 Wavy laminated to domical stromatolites from the Early Archaean Warrawoona Group, Western Australia. Scale in cm.

suggests stratiform stromatolitic laminae . The South African filamentous microfossils coat grains but are not found in a laminated fabric suggestive of stro­ matolitic activity . Unfortunately, no microfossils have yet been found in the more convincing stro­ matolite morphologies . The occurrence of stromatolites in such ancient rocks has great palaeobiological significance . The construction of a stromatolite requires metaboli­ cally, behaviourally, and morphologically sophis­ ticated microbes that interact with a complex of environmental factors . The following phenotypic attributes of prokaryotes are suggested to have evolved by Early Archaean time (and are con­ sidered to be general requirements for stromatolite­ building microbes regardless of their age) : (1) the builder must be benthic throughout most or all of its life cycle . For this to be the case, the microbe has to be denser than the fluid medium and/or develop a means of attachment, like the extracellu­ lar gel (sheaths and envelopes) found in today's stromatolite-building microbes; (2) the microbes must have the ability to trap and/or bind sediment. Sediment incorporation by the growing microbes is required for most stromatolites . Trapping of sedi­ ment is a result of the microbes' growth habit, e . g . cyanobacteria with erect filaments can trap sediment grains between the filaments . Binding can occur with the growth, movement, and extracellular se­ cretions of the microbes . The mucilaginous extra­ cellular secretions help to glue together sediment grains and the microbes; and (3) the benthic organ­ isms must be able to maintain a position at or near the sediment - fluid interface . The photosynthetic physiology is the key solution to this requirement. In addition to sunlight acting as the catalyst for

4 . 7 Stromatolites chemical reactions, it also provides the stimulus for tropisms and taxes. Photosynthetic microbes that build stromatolites orient themselves posi­ tively with respect to sunlight (phototropism) and many move toward sunlight (phototaxis) . Thus by 3500 Ma, microbial evolution was already well advanced . B y Late Archaean time, stromatolites had become more common. Large-scale cratonization occurred during the geological transition from the Archaean to the Proterozoic. This produced relatively stable, shallow marine platforms along the edges of con­ tinents . Cratonization began first in Western Australia and southern Africa. As it continued into the Early Proterozoic, the area open to colonization by stromatolite-building cyanobacteria increased significantly .

The Proterozoic. During this 2000 million year inter­ val of geological time, stromatolites achieved their greatest abundance, the acme of their diversity, and dominated the fossil record . There are numerous unique geometrical arrangements of stromatolite laminae, columns, and branches in the Proterozoic. Analysis of stromatolites (first by Soviet geologists) led to the recognition that certain types of stro­ matolites can be used as index fossils for Proterozoic and Cambrian strata . Unlike most Phanerozoic and Archaean stromatolites, Proterozoic stromatolites are often given binomial names . By Early Proterozoic time, stromatolites appear to have ex­ panded into all their major habitable ecological zones, except for ice-covered regions (stromatolites, however, are associated with late Proterozoic glacial deposits) . By the end of Early Proterozoic time (1600 Ma), all the basic stromatolite architectures had appeared: stratiform, domical, nodular, columnar, columnar­ layered, columnar-branching, conical, and conical­ branching, along with oncolites and possibly thrombolites . Studies of the palaeomicrobiology of the c. 2000 Ma Gunflint Iron Formation in Canada indicate that all classes and orders of modern cyanobacteria had evolved . Columnar, conical, and columnar-branching stromatolites underwent sub­ stantial morphological elaboration and taxonomic diversification during the Middle and Late Proterozoic (1600- 800 Ma) (Awramik 1971 ) . This diversification reached its peak around 1000 Ma (WaIter & Heys 1985) . Columnar and columnar­ branching stromatolites are the forms that best illustrate this increase in diversity and the morpho­ logical complexity that was achieved by stromato-

339

lites (Fig. 6) . High diversity was maintained in the early and middle parts of the Late Proterozoic; however, diversity began to drop sharply c. 680 Ma. Columnar-branching stromatolites and conical stro­ matolites were rare by Early Cambrian time . This decrease in diversity and abundance was probably due to the evolution of grazing metazoans which inhibited the formation of microbial mats, and to burrowing metazoans which destroyed the charac­ teristic fabric of microbially accreted sediments . Meiofauna might have played a major role in the decrease .

The Phanerozoic. The evolution and radiation of Metazoa greatly reduced the abundance and diver­ sity of stromatolites in marine Phanerozoic sequences. Representatives of the group Conophyton (a distinctive conical stromatolite with peculiarities of laminae in the axial zone) are no longer found; elaborately branched columnar stromatolites are rare, as are most other columnar-branching stro­ matolites; domical and columnar stromatolites and oncolites occur and are occasionally locally abundant. Thrombolites (stromatolites that lack lamination and have a macroscopic clotted fabric) became important in the Early Palaeozoic. In addition to the well developed vertical burrows and bioturbated sediments that first appeared in the Early Cambrian, a second eukaryote-induced factor further stressed stromatolite-building microbial communities : the widespread appearance of coarse bioclastic sediment (Pratt 1982) . The evolution of calcium carbonate biomineralization by animals and protists in the Early Cambrian, and the radiation of these organisms, produced significant amounts of bioclastic material, much of it larger than mic­ rite (the dominant carbonate grain size in the

Fig. 6

Middle Proterozoic columnar-branching stromatolite

Baicalia cf. rara from Liaoning Peninsula, China.

340

4 Palaeoecology

Proterozoic and Archaean) . Cyanobacteria are not well adapted to trap and bind coarse-grained ma­ terial (Awramik & Riding 1988) . It is probable that algal eukaryotes combined with cyanobacteria to produce some stromatolites, in particular those composed of silt-sized or larger sediments . Fine­ grained stromatolites, nevertheless, continued to occur and probably dominated the marine Phan­ erozoic record of stromatolites . The Cambrian and Early Ordovician were times of continued stromatolite activity, albeit at reduced levels . Columnar stromatolites, some with branches, domical and stratiform stromatolites, and oncolites were well represented . Microbially bound sediment, at times recognizable by macroscopic stromatolitic ' laminated fabrics, is an important component of Early Cambrian archaeocyathan bioherms (Rowland & Gangloff 1988) . Some thrombolites, which were most abundant during the Cambro-Ordovician, along with laminated stromatolites, built reefs in the Late Cambrian and Early Ordovician . Oncolites were locally abundant, possibly at levels that ex­ ceeded those of the Archaean, Proterozoic, and Late Phanerozoic . Unlike the Proterozoic, when the sub­ tidal realm was the primary site for stromatolite growth, from the Cambrian onward a proportionally large number of stromatolites (in particular those with a stratiform, wavy laminated, and domical morphology) formed in intertidal settings . During the remainder of Phanerozoic time the abundance and diversity of stromatolites became further reduced . A third eukaryote-induced inhi­ bition probably brought this about: the Early ­ Middle Ordovician diversification and radiation of benthic eukaryotic organisms . These metazoans and algae outcompeted stromatolite-building cyano­ bacteria for suitable substrates . Nevertheless, stro­ matolites are not uncommon contributors to reefs and other organic build-ups . In the Late Devonian and Late Permian, for example, reef-like structures composed primarily of stromatolites are known . Stratiform to low dome-shaped stromatolites are not uncommon in intertidal carbonate deposits . The further diversification of benthic green and red algae (for which there are good fossil records) and other algae during the Mesozoic probably further inhibited stromatolite formation . The Phanerozoic non-marine stromatolite record, in particular for the Cenozoic (Fig. 7), is moderately well developed (Monty 1973) . Most non-marine stromatolites appear to have formed primarily as a result of the precipitation of calcium carbonate on and within the microbial mat; allochthonous

Fig. 7 Pleistocene non-marine stromatolites and oncolites from the Koobi Fora Formation, Lake Turkana region, Kenya.

sediment incorporation was a relatively minor phenomenon . Because of the ephemeral nature of fluviatile and lacustrine environments and their general unlikelihood of being preserved for long periods of geological time, the non-marine stro­ matolite record is comparatively poor. All manner of structures occur: columns, branching columns, conical structures, stratiform constructions, domes, and oncolites . Except for the oncolites, most of the constructions are smaller (centimetres in scale) than their marine counterparts (centimetres - metres in scale) . Oncolites, on the other hand, are well rep­ resented by decimetre-sized examples . These large oncolites, however, are usually compound struc­ tures with the top side of the encapsulation charac­ terized by small domes, columns, and branching columns, while the underside contains smooth ­ wavy laminated, occasionally pseudocolumnar layers . The upper side of the oncolite is commonly thicker . Unlike most of the marine oncolites, which formed as a result of the alternation of mobile and stationary conditions, many non-marine oncolites formed in situ .

References Awramik, S . M . 1971 . Precambrian columnar stromatolite diversity: reflection of metazoan appearance . Science 174, 825 - 827. Awramik, S.M. & Riding, R. 1988. Role of algal eukaryotes in subtidal columnar stromatolite formation. Proceedings of the National Academy of Sciences USA 85, 1327- 1329 . Awramik, S . M . , Schopf, J.W. & Waiter, M.R. 1988 . Car­ bonaceous filaments from North Pole, Western Australia: are they fossil bacteria in Archean stromatolites? A dis­ cussion . Precambrian Research 39, 303 -309 .

4 . 8 Reefs and Carbonate Build-ups Byerly, C . R , Lowe, D.R. & Walsh, M.M. 1986 . Stro­ matolites from the 3300-3500 Myr Swaziland Supergroup, Barberton Mountain Land, South Africa. Nature 319, 489 - 491 . Monty, CL .V. 1973. Precambrian background and Phanerozoic history of stromatolitic communities, an overview. Extrait des Annales de la Societe Geologique de Belgique 96, 585 -624. Pratt, B . R 1982. Stromatolite decline - a reconsideration.

341

Geology 10, 512-515. Rowland, S.M. & Cangloff, RA. 1988 . Structure and paleo­ ecology of Lower Cambrian reefs . Pa/aios 3, 1 1 1 - 135 . Waiter, M . R . & Heys, C . R . 1985 . Links between the rise o f the Metazoa and the decline of stromatolites . Precambrian Research 29 , 149- 174. Waiter, M.R, Buick, R & Dunlop, J . 5 . R 1980 . Stromatolites 3400- 3500 m.y. old from the North Pole area, Western Australia. Nature 284, 443- 445.

4 . 8 Reefs and Carbonate Build-ups B . R . ROSEN

Introduction Definition has always been a prominent issue in reef studies, at the heart of which has been the struggle to integrate two perspectives, one based on modern and the other on fossil structures . Although modern reefs provide important insights into pro­ cesses, they can be misleading as gross analogues because of the way in which they have been affected by Quaternary glacioeustatic events - events that cannot be assumed to have applied to all reefs and build-ups throughout the geological record . It is appropriate here to be pragmatic and accept, de facto, all features that have been regarded as reefs and build-ups to date (Scholle et al . 1983; James & Macintyre 1985; Scoffin 1987) . While no simple defi­ nition unites them all, there is a logical (if sometimes indirect) thread that connects them . For a succinct discussion of reef types, see James & Macintyre (1985, p . 22) . Fig. 1 summarizes the principal organic contributors to reefs and build-ups through geo­ logical time . Criteria mentioned in most reef definitions include one or more of the following: organic frame­

build-ups is made at all, reefs are usually thought of as showing evidence of framework as well as relief ('ecological reefs' (Fig . 2B» , whereas build-ups can also be used for relief structures without (observ­ able) framework. Criteria other than framework and relief have come to be regarded as secondary, and may or may not be met in the identification of a particular reef or build-up . However, even this simple approach leaves prob­ lems . Various fossil structures have come to be called reefs simply because their features seem to include framework or relief, in the absence of clear evidence to the contrary. Moreover, the search for Recent analogues of all the different fossil structures now included in reefs and build-ups has generated interest in Recent biogenic structures other than tropical coral reefs, notably deep- and cold-water coral banks, lithoherms, and carbonate mounds (Cairns & Stanley 1981; Mullins et al. 1981; Scholle et al. 1983; James & Macintyre 1985) . These have also become part of the broad notion of reefs and build-ups .

Principal reef criteria

work, raised relief, wave resistance, photic zone restric­ tion, and tropical (or warm water) distribution . In practice, the only structures that can be observed to

Framework. The consensus is that framework (Fig.

fulfil all these criteria are modern tropical coral reefs . All other structures that have been regarded as reefs and build-ups, past or present, usually show (or have been interpreted as showing) either evidence of framework, or raised relief, or both . Generally, if any distinction between reefs and

3) consists of three biogenic components : (1) closely packed, primary in situ accumulations or inter­ growths of rigid macro-organisms (typically corals, branching coralline algae, rudistid bivalves, stro­ matoporoids) further bound together by (2) a secondary framework of in situ encrusting and

342

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cementing organisms (typically coralline algae, bryozoans, and encrusting foraminifera and sheet­ like corals); and (3) infilling material, trapped with­ in this rigid structure, consisting of sediment whose origins may be from either the framework itself or beyond it. There are also numerous infilling organ-

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Fig. 1 Idealized stratigraphic column showing major organic contributors to reefs and build-ups through the Phanerozoic. Block symbols represent framework structures, and open symbols represent structures without framework ('reef mounds' ) . Gaps indicate times when there appear to have been no framework structures, and times when there were no build-ups at all . Note that many authors would regard skeletal algae as being similar in importance to corals in the Tertiary. (After James in Scholle et al. 1983, by permission from the American Association of Petroleum Geologists. )

isms, usually smaller than the main framework contributors, both encrusting and free-living, many of them (coelobites) occupying caves, cavities, and overhangs (cryptic habitats) . Much sediment infill is also postlithification. This rigid framework model, however, is an idealized end-member of a whole spectrum of 'frameworks' . Different processes of sedimentation and preservation result in an intergradation of pro­ minence between the above three framework com­ ponents . Large branching or mound-like organisms may be sparse or absent, leaving encrusting and cementing organisms like coralline algae to build up structures on their own (Bosence 1983; Scholle et al. 1983), as in the largely algal Bermuda cup reefs . Encrusters can also bind sediment ranging in grain size from fine mud and silt (as in stromatolites) to cobbles of broken, worn, and transported material, or other accumulations of biogenic clasts like rho­ doliths . If the clastic material consists of large, re­ latively unworn coral fragments, it may be hard to distinguish the finally preserved rock from a true in situ framework of macro-organisms . At another extreme (and probably more abundant than the idealized framework model), dense stands or ac­ cumulations of organisms can occur without any apparent binding organisms, e . g . the coral beds of the British Carboniferous and many fades of ru­ distid reefs . In the case of lithoherms, early dia­ genesis has a significant constructional role not

4 . 8 Reefs and Carbonate Build-ups unlike a framework built by organic encrusters, but in this case, primary structure consists almost en­ tirely of sediment; the organic component consists of secondary colonizers . While a true framework is usually considered to be a relatively permanent feature, frameworks of non-rigid organisms are also very important as con­ structive agents, although they usually break down before preservation. Structures of this kind, built up by sediment-trapping marine grasses, occur in the inshore areas of the Florida Keys (Scholle et al . 1983; James & Madntyre 1 985, Bosence et al. 1985) . Delicate branching corals, crinoids, and organisms whose preservable skeletal elements are held together by soft tissues (such as many sponges and octocorals) can also have a similar sediment­ trapping role, but usually break down into frag­ ments and spicules before preservation . The environment of such non-rigid frameworks is gen­ erally less favourable to cementing organisms than that of rigid frameworks, so the resulting rock contains large amounts of sediment in relation to primary organisms . Even with rigid frameworks, however, the final proportion of framework in the resulting rock can be surprisingly reduced to shadowy remnants where they have suffered extensive in situ contemporaneous destruction by boring organisms (such as endolithic algae, clionid sponges, and various bivalves) . Diagenetic processes can also destroy framework . Thus the concept of framework, like that of reefs, has become broad, and takes into account both frameworks that are preserved and those that are not. The end-product may be a structure with relief but no apparent framework, a framework with raised relief, or a framework without true relief (i . e . a laterally developed i n situ growth or biostrome) . There are also relief-features to consider that may never have had any framework at all, as discussed next .

Relief. For fossil build-ups, the identification of relief is usually an inference derived from the ob­ servation of a fades discontinuity that marks the limits, ideally, of a bioconstructional formation. Relief is inferred if this discontinuity has a mound­ or ridge-like geometry, and (in theory at least) it results from the ability of framework organisms to maintain net growth against the agents of destruc­ tion and transport . In many cases, moreover, it is difficult to conceive what other primary sedimen­ tary process could cause the commonly observed steepness of sedimentary dips. Problems arise from

343 Process P r i m a ry framewor k g rowth - - - - - - 20 Boring & e n c r u stat i o n 60 Loose 80 sed i ment acc u m u l a t i o n

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Fig. 3 Vertical cross-section through part of a Bermuda lagoonal patch reef, showing framework structure and internal processes. Capital letter symbols indicate primary framework of scleractinian corals, here consisting of three genera (D, Diploria; M, Montastrea; P, Porites). Secondary framework (laminated pattern) consists of coralline algae above, Bryozoa in middle cavities, and Agaricia coral in lower cavity. The encrusting foraminiferan, Homotrema, lines undersides of overhangs . Sediment infill is shown by horizontal stipple. Bioerosion is denoted in black: mainly by bivalves like Lithophaga (larger holes) and clionid sponges (smaller holes); not to scale . (After Scoffin 1987. )

this, however: 1 Some of the relief and its flank-slope steepness may be due to antecedent structure (Fig. 4, and discussed below) . 2 There are relief features that contain no clear framework. This might be because framework has not been preserved, or because the build-ups were shaped primarily by contemporaneous hydro­ dynamic factors or early diagenesis . (Such features can also be colonized by organisms as they grow, giving the illusion of framework. ) 3 Postlithification erosion can 'create' o r enhance primary relief. It is not always easy to distinguish a discontinuity surface which is due to strati­ graphical disconformity from a syndepositional interface between framework and flanking fades, espedally when identification of framework is un­ certain. Similarly, the present-day surface of land erosion can also 'create' reef-like relief in andent deposits, and this is not easy to distinguish from the exhumation of andent syndepositional features . Although emphasis has been placed on the recog­ nition of talus blocks to infer syndepositional relief,

344

4 Palaeoecology

Fig. 4 Composite structure and antecedent surfaces as factors in reef relief (not to scale) . A, Recent model showing Holocene reef growth as a veneer, 0 - 1 0 m thick (black), overlying disconformity in karst-eroded, pre-Holocene reef limestones . (After Braithwaite 1987. ) B, Fossil reef structure composed of a stacked series of reef phases separated by discontinuitiesi lower discontinuity (K) is a karstic erosion surface, while upper discontinuity (H) is a hardground. (After James & Macintyre 1985 . )

this kind of evidence can be misleading. Blocks at the foot of modern deep fore-reef slopes in the Caribbean, previously taken to be modern and syndepositional, might well be residuals derived from subaerial erosion of older reef limestones during pre-Holocene low sea-level stands . Many ancient talus deposits might therefore have origi­ nated in analogous fashion. Better knowledge of Pleistocene - Holocene karstic phenomena and the erosional history of modern reef complexes (below) has stimulated a search for intraformational palaeo­ karstic surfaces in fossil build-ups (Fig. 4) . This has revealed that at least part of the apparently contem­ poraneous relief of some supposed build-ups may actually be due to cyclical alternation of deposition of prograding carbonates with emergence and karstic erosion . 4 Another possible cause of 'pseudo-relief' is that of sharp syndepositional interfaces between differ­ ent communities and facies . Where the relative lat­ eral extent of these interfaces persists, waxing and waning through time, a mound-like geometry can develop, although at the time of deposition, one facies may not have projected significantly more than another above the sea floor ('stratigraphic

reefs' : Fig . 2A) . Other postdepositional factors, such as diagenesis and relative compaction, may also account for 'pseudo-relief' or exaggerate primary relief. Even in modern environments, reef relief, though readily observed, is not a simple phenomenon. It is certainly not always attributable to framework or sediment-trapping organisms . Hydrodynamic in­ fluence can be as important as the direct role of organisms, or more so, as in the growth of columnar stromatolites, and in the linear carbonate mud mounds of Florida Bay (now regarded as partial analogues of Carboniferous Waulsortian reefs; Bridges & Chapman 1988) . A great deal of apparent relief, moreover, can be ascribed to underlying, antecedent topography (Fig. 4) . This is now beyond doubt for most modern coral reefs, for which glacioeustatic events have been especially important . Shallow drilling and radio­ metric dating show that in both scale and detailed topography, much of their relief still matches the dissected and cavernous morphology of pre-existing platforms formed by underlying, older reef lime­ stones . These were evidently exposed subaerially during glacioeustatic regressions, especially dur­ ing the last 140 000 years, and subjected to karstic erosion . Since then, the Holocene transgression has drowned the resulting topographies, and renewed modern growth has contributed only a veneer (varying from a few centimetres to about 10 m or more) which often scarcely masks these older features (Fig. 4A) . Recognition of this took a sur­ prisingly long time and was hindered by: (1) the lithological similarity between modern and older limestones; and (2) the fact that some of the older limestones were prograded to approximately the same sea-level as today, so the uppermost features of modern reefs are in fact partly contemporary and partly fossil. Implications of this for the study of fossil reefs are as follows : (1) they may similarly have been affected by intraformational, erosional histories (Fig. 4B) that are not immediately obvious and might still be unrecognized; and (2) the most informative modern analogue for fossil reefs is not the gross structure and relief of modern reefs, since this is usually a composite of numerous phases which may go back to the Early Tertiary or before . Rather, it is the Holocene veneer alone that provides the most direct clues for a single phase reef-growth model . How­ ever, even this has limitations as a general case for the fossil record, because it represents a relatively short term response to transgressive conditions . It

4 . 8 Reefs and Carbonate Build-u ps must be adapted to take account of the probable effects of static or regressive sea-levels, as well as different rates of sea-level change and the vertical component of any tectonic movement that affected the foundations . Even without eustatic influence i n the history o f a build-up, the ecological preference of many ben­ thic organisms for sea-floor highs (like submarine horsts, scarps, and volcanoes), as well as the greater rates of carbonate deposition on such features, points to a general likelihood of an antecedent factor in almost any carbonate complex. In order to relate relief in fossil build-ups to that of modern reefs, physical scale must also be con­ sidered . Many modern coral reefs are extensive complex structures many kilometres across with a whole mosaic of carbonate facies . True framework is highly localized, not necessarily at the seaward rim of such complexes, and usually accounts for much less surface area and volume than bioclastic sediments, oolites (e . g . Bahamas), and evaporites . This facies complexity appears t o reflect immaturity, because Holocene submergence and growth recov­ ery has been so recent, and this is another constraint to be considered in using modern reefs as fossil analogues . Although some fossil build-ups are also seen as complexes (e .g. the Devonian of the Canning Basin), many are defined purely with respect to a local outcrop of a framework or relief feature, perhaps only metres across (e . g . the Silurian of the British Wenlock) . The best analogues for such structures are not complete reef complexes like modern atolls, which are tens of kilometres across, nor even plat­ form reefs like those of the Australian Great Barrier Reef complex, but rather the separate small-scale constructional features within these carbonate sys­ tems . The lagoonal patch reefs of Bermuda, which are just one of a whole range of features within its atoll-like complex, are much more comparable in scale and structure to reefs of the British Wenlock. Similarly, there is confusion of scale in the use of 'lagoon' in reef studies, which might denote any­ thing from the shallow (less than 5 m) sheet of water that covers many modern reef flats, to the large and relatively deep (up to 70 m or more) areas that lie within atoll rims or between barrier reef complexes and their mainland . It follows that 'fore-reef' and 'back-reef' concepts also have various meanings . It is probably best to think of reef relief as a fractal phenomenon - similar topographic patterns re­ peated within themselves on different scales (e . g . compare atolls, faros, and microatolls) .

345

Other criteria Remaining criteria are secondary, often introduced in support of a particular reef interpretation . Although such criteria apply to modern coral reefs, there also exist modern bioconstructional features and other possible analogues of ancient build-ups that occur: (1) below wave base; (2) below the photic zone; (3) in deep and cold water; and (4) in high latitudes . Many kinds of largely algal build­ up, sometimes combined with bryozoans, occur in temperate latitudes, and there exists a whole suite of different deep- and cold-water coral banks (Cairns & Stanley 1981 ; Mullins et al . 1981; Bosence 1983; Scholle et al . 1983; James & Macintyre 1985; Scoffin 1987) . Common arguments for inferring wave influence are : (1) relief as an indication of wave resistance; and (2) zonation of communities as a response to sharp environmental gradients caused by the breakwater-like effect of a positive feature close to sea-level. But relief is equivocal evidence, as already discussed, and zonation can occur in deeper-water structures . Conversely, modern small surface patch reefs of a size comparable to many fossil build-ups are often too small to show either real zonation or any clear fore-reef and back-reef differences . In view of the popular use of reefs and build-ups as palaeoclimatic and palaeogeographical indicators, it is therefore also worth noting that their occurrence (defined broadly) in the geological record is not a reliable reflection of temperature, climate, latitude, water depth, or wave energy, even when corals or algae are prominent.

References Bosence, D.W.J. 1983 . Coralline algal reef frameworks . Journal of the Geological Society 14, 365 -376. Bosence, D.W.J., Rowlands, R.J. & Quine, M . L . 1985. Sedi­ mentology and budget of a Recent carbonate mound, Florida Keys. Sedimentology 32, 317-343 . Braithwaite, c .J.R. 1987. The structure and history of Recent reefs . Geology Today 3, 197-20 1 . Bridges, P.H. & Chapman, A.J. 1988. Sedimentology of a deep water mud-mound complex to the southwest of the Dinantian Platform in Derbyshire, U.K. Sedimentology 35, 139 - 162. Cairns, S.D. & Stanley, G . D . , Jr. 1981 . Ahermatypic coral banks: living and fossil counterparts. Proceedings of the 4th International Coral Reef Symposium 1, 61 1 - 61 8 . James, N.P. & Macintyre, I . G . 1985 . Carbonate depositional environments, modern and ancient. Part 1 : reefs : zonation, depositional facies, diagenesis . Colorado School of Mines Quarterly 80(3), i -ix, 1 - 70 .

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4 Palaeoecology

Mullins, H.T., Newton, CR., Heath, K. & Vanburen, H.M. 1981 . Modem deep-water coral mounds north of Little Bahama Bank: criteria for recognition of deep-water coral bioherms in the rock record. Journal of Sedimentary Petrology 51, 999 - 1013.

Scholle, P.A., Bebout, D.C & Moore, CH. (eds) 1983. Carbonate depositional environments. Memoir of the American Association of Petroleum Geologists, No. 33 . Scoffin, T.P. 1987. An introduction to carbonate sediments and rocks . Blackie & Son, Bishopbriggs, Glasgow.

4 . 9 Encrusters P . D . TAYLO R

Introduction Encrusting animals and plants are important colon­ izers of marine hard substrata today (Jackson 1983), and are well represented in the Phanerozoic fossil record. Interest in modem encrusters is linked both to their commercial importance as foulers of man­ made structures (e . g . ship's hulls and offshore oil platforms), and to the fact that encrusting com­ munities on artificial settlement panels are excellent subjects for studies of competition and ecological succession. Encrusters are also attractive subjects for palaeoecological studies because they retain their original spatial relationships to the substratum and to one another, thus allowing the inference of life orientations and interactions . Furthermore, the substrata used by encrusters are often discrete and of a size suitable for collection in the field and transportation back to the laboratory for detailed study. Communities living on hard substrata are usually dominated by sessile organisms which include endobionts (boring into the substratum) and epibionts (attaching to the surface of the substratum) . The epibionts comprise organically-attached (e . g . pedically-attached brachiopods, bysally-attached bivalves) and cemented forms. Many organisms have cemented bases or holdfasts which anchor more extensive erect parts (e . g . crinoids, arborescent bryozoans) . However, the term 'encruster' is here restricted to organisms of low profile which are cemented to the substratum across a large part of their basal surfaces . Organisms cementing to small substrata which they quickly outgrow to rest freely on the sea bed (e . g . gryphaeate oysters, many

stromatoporoids) are excluded from this definition of encrusters, although, as with erect organisms, they may intergrade with typical encrusters . Encrusting animals are characteristically suspen­ sion feeders, capturing particulate food from the water column . Being sessile as adults, they are de­ pendent for colonization on a free-swimming larval stage . Those individuals whose larvae settle suc­ cessfully and survive immediate post-settlement mortality are termed recruits .

Taxonomic composition and morphology of encrusters The following groups generally dominate modem encrusting biotas: algae, foraminifera, sponges, coelenterates, bryozoans, brachiopods, bivalves, serpulid polychaetes, ascidian tunicates, and bar­ nacles. Apart from ascidians, all of these groups contain at least some species with mineralized skel­ etons, and therefore have good preservation poten­ tial. Even soft-bodied encrusters are occasionally preserved as fossils by bioimmuration, i . e . when overgrown by other encrusters and left as natural moulds on their undersides . I t i s useful t o classify encrusting animals accord­ ing to aspects of their growth and form that deter­ mine how they use and compete for substratum space . A fundamental distinction is between solitary and colonial forms . Solitary forms typically grow to a fixed size and shape (determinate growth), whereas colonial forms, which grow by the asexual budding of modular units (zooids), are often highly irregular in size and shape (indeterminate growth), may suffer partial mortality (death of some but

4 . 9 Encrusters not all zooids in the colony), and undergo fission into several parts or fusion with other colonies (Section 4.6) . Encrusters commonly found as fossils are shown in Fig. 1 . Solitary encrusters fall into two main morphological groups : forms with a subdrcular outline shape which grow centrifugally from an encompassing growing zone, and linear forms which grow in straight, curved, or spirally coiled lines from an apical growing zone . Subdrcular forms are often bivalved or multiplated, and are well equipped to defend their margins against lateral overgrowth by other encrusters . Many linear forms can change growth direction and 'migrate' signifi­ cantly across the substratum, but they have poorly defended flanks which are vulnerable to lateral overgrowth . Colonial encrusters also fall into two main mor­ phological groups Oackson 1979) : sheets (Fig . 2A), which are 'two-dimensional' colonies, with closely­ packed zooids, which spread across the substratum by zooidal budding from an encompassing grow­ ing zone; and runners (Fig. 2B), which are 'one-

347

dimensional', branching colonies which grow by budding zooids from numerous growth tips . Sheet­ like colonies are highly committed to defending and winning substratum space from other encrusters (confrontational or phalanx strategy) . Runners, by contrast, are vulnerable to lateral overgrowth, but distribute their zooids across wide areas of the sub­ stratum (fugitive or guerilla strategy); this enables them to locate patches of substratum (spatial refuges) where the probability of mortality is lower and in which some zooids may survive (see also Section

4.6) . Points to note in the geological history of encrust­ ers (Fig . 1) are the major radiation of encrusters in the Ordovidan, the scardty of encrusters in the Late Palaeozoic, and the Mesozoic radiation of the modem encrusting biota, with the late appearance of acorn barnacles .

Encruster- substratum relationships Modem communities of encrusters are best known from intertidal and shallow subtidal habitats, and

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Fig. 2 Encrusting animals and their interactions. A, Sheet-like cheilostome bryozoan Schizoporella growing towards a polychaete tube Spirorbis and a small barnacle; Recent, Adriatic Sea ( x 10) . B, Linear growth-form in encrusting foraminifers Nubeculinella; Upper Jurassic, Normandy, France ( x 42) . C, Reciprocal overgrowth between a sheet-like sponge and a runner­ like cyclostome bryozoan; the upper part of the sponge is overgrowing the branch flanks of the bryozoan, but a branch of the bryozoan is overgrowing the sponge at the bottom left; Upper Cretaceous, Norfolk, U.K. ( x 14) . D, Spirorbis fouling the surface of the cyclostome bryozoan Sagenella; Silurian, Gotland, Sweden ( x 57) . E, Runner-like tabulate Aulopora, partly overgrown by the basal holdfast of a cryptostome bryozoan, encrusting the epitheca of a solitary rugose coral; Silurian, Gotland, Sweden ( x 3) . F, Dense encrustation of serpulid polychaetes on a cobble; Middle Jurassic, Gloucestershire, U.K. ( x 1 .4) .

4 . 9 Encrusters include communities attached to rocks, shells and skeletons of living and dead animals, macroalgae, and artificial substrata (e . g . pier pilings) . Organisms which attach to living plants are termed epiphytes; those attached to living animals are termed epizoans . Epiphytic communities of nearshore macroalgae have been extensively studied, but macroalgal epi­ phytes have yet to be recognized in the fossil record. Epizoic communities can be found at the present day on a wide variety of hosts, particularly sessile animals (e . g . large epifaunal bivalves, undersides of corals) . Colonization by epizoans can be advan­ tageous or disadvantageous to the host animal. For example, some Recent bivalves gain from the camouflage provided by epizoans, but it has been shown that certain epizoans increase drag and therefore the probability of dislodgement. The term 'epizoan' should be applied only to encrusters whose hosts were alive at the time of encrustation, although inference of life association can be extremely dif­ ficult in fossils (one of the few reliable criteria is epizoan-induced modification of host growth pattern; Section 4. 14) . Encrusted skeletal substrata are very common in the fossil record and range from intact, in situ skel­ etons of probable living hosts, to fragmented, trans­ ported, and remanie skeletal debris . The condition of encrusted substrata can provide useful infor­ mation on depositional environments, particularly on the occurrence of episodic sedimentation and reworking. Among studied hard substrata are : Palaeozoic stromatoporoids, which frequently har­ bour encrusting biotas on the cryptic undersides of their coenostea; cavities in reefs occupied by coelobionts; and Cenozoic molluscan shell gravels in which the concave inner surfaces of bivalves may be particularly well encrusted. In environments normally hostile to epibenthos, as in some muddy deposits, the rare substrata provided by the shells and bones of nektonic animals (e . g . cephalo­ pods, marine reptiles) constitute important habitat islands for sessile species which often form dense encrustations . Abiotic substrata for encrusting organisms range from rocky shorelines to hardgrounds, pebbles and cobbles, and even coarse sandy sediments . Coloni­ zation of ancient rocky shorelines has seldom been recognized, but a good example occurs in the Upper Cretaceous of Sweden where Surlyk & Christensen (1974) described zonation in encrusted boulders of Precambrian gneiss . Hardgrounds formed by early lithification of carbonate sediments are better known as substrata for encrusters (Palmer 1982) .

349

Hardground morphology determines the types of habitats they provide . Upper surfaces may be planar or hummocky, and the hardground can be undercut, broken-up, or penetrated by burrows excavated before the sediment was lithified . Hummocky Ordovician hardgrounds commonly lack encrusters on the hummocks but are colonized by bryozoans and other encrusters between the hummocks . Undercut and burrowed hardgrounds commonly show a polarization of encrusters between exposed upper surfaces and cryptic undersides or burrow walls . Trends through the Phanerozoic in hard­ ground assemblages have been towards: (1) greater diversity of cryptic inhabitants of hardgrounds; (2) replacement of encrusters on hardground surfaces by borers; and (3) an increase in the proportion of encrusters with exoskeletons . These trends may re­ flect the increasing influence of grazing predators . Clasts of widely ranging size and derived from various sources (including broken-up hardgrounds, and exhumed concretions - 'hiatus concretions') frequently support encrusting biotas. While the surfaces of cobbles and pebbles in high energy environments may be very stressful habitats, cavi­ ties and vacated borings in these clasts can act as important refuges for encrusters . On the micro­ scopic scale, the larvae of many encrusters pref­ erentially settle in cracks and crevices (rugophilic behaviour) . Encrusters of in situ substrata may be found to exhibit orientated growth, e . g . the commissures of encrusting bivalves and brachiopods often point downslope, presumably allowing unwanted particles to be more easily expelled .

Competition, aggregation, succession, and disturbance Living space is often a limiting resource which is actively competed for by organisms inhabiting hard substrata today. Even when free space appears to be present (as in most fossil assemblages), the chance juxtaposition of encrusters may cause interference competition . A great deal of research has been published on spatial competition among living encrusters (see Buss 1986), and there is much con­ troversy about its influence on community compo­ sition relative to such factors as composition of the larval pool, disturbance, and predation. Encrusters compete for space by overgrowing the margins (lateral overgrowth) or settling on the surfaces (fouling) of other encrusters, by releasing toxic chemicals, or by prising competitors off the sub-

350

4 Palaeoecology

stratum . Settlement panel studies have shown a decrease in spatial competitive ability from ascidians to sponges, to bryozoans, to serpulids and barnacles . However, details of spatial interactions in specific communities can be very complex, and rarely is there a simple competitive hierarchy (i . e . species A overgrows B , and both A and B overgrow C, etc . ) . Overgrowth interactions between pairs of species can be intransitive (i. e . species A some­ times overgrows B, but sometimes B over-grows A), reciprocal overgrowth (Fig. 2C) may occur between individuals (i. e . individual A overgrows B along part of their contact, but B overgrows A elsewhere), and growth of both competitors may cease at their contact (stand-off) . Such interactions are better expressed in the form of a competitive network. Overgrowth does not always result in mortality; colonial animals typically survive over-growth of some of their zooids (Section 4 . 6), and overgrowth of exoskeletons may leave the feeding parts of some organisms free to function (epizoism) . Certain morphological features correlate with success in spatial competition . Sheet-like colonies and subcircular solitary encrusters have well de­ fended margins and can often overgrow runner-like colonies and linear solitary encrusters . Other attri­ butes which can aid overgrowth include large body size (especially thickness, increased by the frontal budding of zooids in some colonial encrusters), rapid growth rate, spinosity, and the ability to raise margins above the substratum or to redirect growth to encounter competitors 'head-on' . Many organ­ isms strongly resist fouling of their surfaces by larvae, and may therefore pre-empt substratum space if they are able to recruit early and grow rapidly . The study of spatial competition in fossil assem­ blages is hampered by time-averaging; determining whether the encrusters lived contemporaneously can be a major problem. Superimposition of indi­ vidual A on individual B can mean either: A suc­ ceeded B in time and overgrew B's dead skeleton; or A competed successfully for space with B. Only when reciprocal overgrowth is observed (Fig . 2C), or competitor-induced modification of skeletal mor­ phology can be inferred, is it possible to demon­ strate that the individuals were contemporaneous . Nevertheless, spatial competition among ancient encrusters clearly did occur, both by lateral over­ growth and fouling (Fig. 2D), and was apparently very similar to that among modern encrusters, although often involving very different groups of organisms (see Taylor 1984) . As in the Recent, sheet-

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Aggregation of conspecifics (Fig. 2F) i s a common feature of encrusters (e . g . barnacles, spirorbid serpulids) . The mechanisms by which aggregation is achieved vary and include selective settlement of larvae close to adult conspecifics (gregarious behaviour) and differential mortality of settlers . Among the demonstrated or suggested advantages of aggregation are greater probability of outbreed­ ing, increased success in interspecific competition for space, and enhanced feeding ability. Temporal changes in the composition of encrust­ ing biotas on settlement panels have been widely investigated . Classic models of ecological succession which were developed for terrestrial vegetation view early colonizers as 'paving the way' for later colonizers by modifying the habitat. However, many encrusters inhibit later colonizers, and suc­ cession often depends more on the lifespans of individual species, with long-lived species replac­ ing short-lived species through time, and also on their spatial competitive abilities . An initial increase in species diversity can be reversed in later stages if one or a few competitively dominant species are present . In some communities (e . g . cryptic coral reef habitats) there is an overall tendency for solitary species to be replaced by colonial encrusters, but in others (e .g. temperate shallow subtidal habitats) the reverse sequence is found . Of relevance to palaeo­ biological studies is the increasing proportion of non-fossilizable soft-bodied encrusters found during succession in a tropical cryptic community (Rasmussen & Brett 1985) . Disturbance can be an important factor in the development of encrusting communities . Agents of disturbance include grazing predators (especially echinoids), sediment scour, and overturning of substrata by currents and mobile animals . In gen­ eral, disturbance 'arrests' succession by preventing superior spatial competitors from achieving domi­ nance . Macroinvertebrate grazers, for example, allow grazer-resistant but competitively subordi­ nate algae to flourish on some hard substrata . Osman (1977) found that rocks o f intermediate size (1 - 10 dm2) supported the highest diversities of encrusters because they were disturbed by wave currents too often to prevent their domination by species of high competitive rank but too seldom to prevent their colonization by a large number of species . An Ordovician cobble-dwelling biota o f en­ crusters provides a good example of how succession

4 . 1 0 Ancient Plant Communities may have been affected by disturbance (Wilson 1985) . Stabilized cobbles became dominated by the sheet-like bryozoan Amplexopora, which overgrew all other encrusters, whereas periodically disturbed cobbles developed high diversity assemblages because Amplexopora had insufficient time to over­ grow the other encrusting species . Bioerosion as a form of disturbance is evident on many post­ Palaeozoic substrata that are marked by the grazing traces of echinoids (Gnathichnus) and of gastropods and chitons (Radulichnus) . Future studies of fossil encrusters promise to progress beyond the description of individual assemblages to comparative studies of assemblages through time which may shed light both on long­ term ecological changes, and on possible coevol­ ution between competitors for substratum space .

References Buss, L.W. 1986. Competition and community organization on hard surfaces in the sea. In: J. Diamond & T .J. Case

351

(eds) Community ecology, pp. 517-536 . Harper & Row, New York. Jackson, J . B . C . 1979 . Morphological strategies of sessile animals. In: G. Larwood & B . R Rosen (eds) Biology and systematics of colonial organisms, Systematics Association Special Volume 1 1 , pp. 499- 555. Academic Press, London. Jackson, J . B . C . 1983. Biological determinants of past and present sessile animal distributions . In: M.J.5. Tevesz & P.L. McCall (eds) Biotic interactions in Recent and fossil benthic communities, pp. 39- 120. Plenum, New York. Osman, RW. 1977. The establishment and development of a marine epifaunal community. Ecological Monographs 47, 37- 63 . Palmer, T.J. 1982 . Cambrian to Cretaceous changes in hard­ ground communities . Lethaia 15, 309- 323. Rasmussen, K.A. & Brett, C . E . 1985 . Taphonomy of Holocene cryptic biotas from St. Croix, Virgin Islands : information loss and preservational biases. Geology 13, 551 -553 . Surlyk, F. & Christensen, W.K. 1974. Epifaunal zonation on an Upper Cretaceous rocky coast. Geology 21, 529- 534. Taylor, P.D. 1984. Adaptations for spatial competition and utilization in Silurian encrusting bryozoans. Special Papers in Palaeontology 32, 197-210. Wilson, M.A. 1985 . Disturbance and ecologic succession in an Upper Ordovician cobble-dwelling hardground fauna. Science 228, 575 - 577.

4 . 10 Reconstructing Ancient Plant Communities A . C . S C OTT

Introduction Terrestrial vegetation comprises a diversity of plant communities, the majority of which live in erosional rather than depositional areas. In addition, during the life cycles of the constituent plants, organs such as leaves and seeds are shed and may be trans­ ported, buried, and preserved far from the growth site . Different plant parts may behave in various ways during transport by wind or water, and decay rates may also vary, depending on their original plant chemical composition (Scott & Collinson 1983; Ferguson 1985) (Fig . 1) . Consequently, the recon­ struction of ancient plant communities from fossil assemblages is fraught with hazards. One major problem is a general lack of knowledge of whole plants; relatively few have been reconstructed in

total, combining roots, stems, leaves, and fertile organs . There are several approaches to fossil plant ecology, both biological and geological. Detailed morphological and anatomical studies of plant fossils can yield ecologically significant data con­ cerning form or life habit. For example, a thick cuticle may imply a xeromorphic (dry) habitat, while specialized cells in roots may indicate life in a waterlogged environment . Geological observations may distinguish in situ vegetation from drifted plant assemblages . In order to use this geological data, methods of qualitative and quantitative data collection should be carefully considered (Scott & Collinson 1983) . The plants have undergone trans­ port, deposition, and diagenesis before collection, and a series of interpretive steps must be taken

352

4 Palaeoecology

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Problems in relating fossil plant assemblages to contemporaneous plant communities . Initiators of the fossilization sequence (on some or all of the plants in a community) : 1, internal factors, such as organ abscission, organ shedding, disease, and resistance of plant organ to decay . 2, external factors, such as animal destruction, storms, floods, land subsidence, climatic change, erosion, other natural catastrophies (e .g. forest fires), and proximity to site of transport. Key factors controlling fossil plant assemblages (affecting some or all of the plants in the fossilization sequence) : destructive mechanisms, such as (a) decay, (b) mechanical break-up, (c) immediate post­ depositional reworking, (d) diagenesis, (e) weathering, and (f) collecting bias; and interference, such as (g) sorting, and (h) additions from other communities . (From Scott 1977.)

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Important data come from the study of in situ veg­ etation, but even here the plants preserved may be highly selected . Two types of in situ plant assem­ blages are generally encountered: fossil forests and peats (coals) . Upright trunks occur widely both geo­ graphically and stratigraphically; well known examples include the Tertiary forests in Yellows tone National Park, U . S . A . and the Purbeck fossil forests in southern England . In both cases the trees com­ prise only trunks preserved as silica permineraliz­ ations or petrifications; leaves or reproductive

structures are not usually found attached, and gen­ erally only the bases of the trunks survive . Similarly, few non-arborescent plants are preserved; her­ baceous forms are especially poorly represented because they decay quickly. More diverse assem­ blages are preserved in peats and coals but they represent specialized wetland floras (Broadhead 1986) . Only a selection of the original plant com­ munity is preserved, because of selective decay during the peat-forming process. Only if perminer­ alization (Section 3. 10) took place early in peat formation is a more complete community preserved, e . g . the Rhynie Chert from the Lower Devonian of Scotland and Upper Carboniferous coal balls of Europe and North America . Studies of coal balls from several levels through coal seams have allowed the identification of numerous plant communities . Such data, together with considerations of repro­ ductive structures (particularly of the lycopods) have generated hypotheses concerning the relative water table during peat formation . The interpretation of drifted plant assemblages is even more difficult. Plants become incorporated into the sedimentary record in a variety of ways. Leaves, branches, and fertile organs may be nat­ urally abscissed or broken from the plant by storms or fire . These fragments may be carried by wind and if they reach water may be transported into a depositional environment. Most plant material decays before reaching water, or during transport. Of the original plant community, only a small number of species may survive and be represented by a restricted number of parts (Spicer 1989) . Obvi­ ously plants living near water have a greater chance of being represented, but even then much depends on differential decay, e . g . conifer needles with thick cuticles survive transport and deposition more easily than herbaceous plants (such as grasses) which decay where they grow . The fossil record is very biased toward wetland plants, which are more resistant to decay. Many assemblages, however, represent plant litter incorporated into rapidly deposited sediment following storms and floods (Fig. 2) . Our interpretations of fossil plant assemblages have benefited much from taphonomic studies of Recent material, including studies on the modern analogues of ancient depositional settings, such as deltas and lakes (Spicer 1989; Scheihing & Pfefferkorn 1984; Collinson 1988) . Plant assemblages found in various sedimentary settings have been compared to the surrounding vegetation. In addition, experi­ mental studies of decay, break-up, transport, settling

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rates, and preservation have emphasized that only a small proportion of the original vegetation, derived from several sources, may become fossilized .

353

Much data may be obtained from the enclosing sediments. Facies studies aid interpretation of the depositional environment and provide data con­ cerning the transport history. Identification of storm layers and of the mixing of plant material from different sources is important, but is often difficult to achieve . Layer by layer collecting and recording of plant material is of major value (Scott & Collinson

1983) . Even after burial there is potential for further alteration, with decay by bacteria and fungi con­ tinuing and causing further selection. However, when the organic material of the plant decays, an impression may be left. Early permineralization by pyrite, calcite, or silica may lead to anatomical preservation (Section 3 . 10) . Compaction after burial may cause two originally separated plant organs to become closely associated. Equally, two successive layers of plant remains may have had quite dif­ ferent origins and histories (Fig. 2). Despite these problems there are several approaches to the study of fossil plant ecology, including field observations, laboratory, and experimental studies . Field and laboratory data gathering

Data collection in the field is of prime importance . This may be quantitative (such as percentage cover or volume), semiquantitative, or qualitative (present/absent, common- abundant, etc . ) . The data may be handled in several different ways: presented purely in tabular form or, e . g . , as histograms, or handled statistically using a variety of techniques (including principal component analysis, dis­ criminant analysis, or correspondence analysis) . Whatever collecting method i s chosen, bed by bed recording is essential, as is the recording of detailed sedimentological data. The methods employed, such as the use of quadrats, will depend on the type of exposure and a consideration of what is to be achieved . Bulk collections are advisable . Interpretation of sedimentological data is equally important and may concern process, depositional environment, and transport history of the plants . Taphonomic studies are also necessary, including an analysis of size and the type of organ present, potential preservational bias, and the occurrence, for example, of charcoal (Scott & Collinson 1983; Broadhead 1986) . In the laboratory the methods used depend on the type of preservation. Where plant assemblages comprise mainly leaf compressions, simple splitting of the rock may suffice . Where abundant small

354

4 Palaeoecology

plant organs (such as fruits and seeds) occur, dis­ aggregation of the sediment and sieving may be required . Where permineralizations occur (such as in limestones and other lithified rocks) beds must be cut into slabs and peeled. Comparing data from these three types of deposit can be difficult. Experi­ mental studies of transport (involving a flume) or compression can yield data significant for the interpretation of the assemblage . Only when all these studies are complete should a vegetational reconstruction be attempted .

The ecology of ancient plant communities Reconstruction of whole plants is a major problem and depends on finding connections between plant parts . Common associations may only reflect sedi­ mentological criteria but, if anatomical features are also shared, may prove acceptable evidence . Many reconstructions of ancient vegetation contain poorly reconstructed plants based on unsatisfactory evi­ dence (Collinson & Scott 1987) . There are relatively few fully reconstructed plant species, although a general idea of what others looked like is known . Reconstructing the ecology of ancient plant com­ munities is difficult and opinions differ amongst specialists on how far it is possible to go . Vegetation has been reconstructed not only from in situ plant assemblages but also from fossil soils and drifted assemblages . Guiding principles must be : (1) collect accurate data; (2) interpret the data, knowing its limitations; and (3) finally produce a hypothesis concerning the plant communities . The acquisition of new data may, therefore, necessitate the develop­ ment of new hypotheses. In some cases (such as peats or coals), successive changes in vegetation can be established . Plant communities have often been used to interpret climatic regimes and both short- and long-term change in climate (Section 4 . 1 9 . 1 ) . Changes in peat-forming vegetation in the Upper Carbonifer­ ous coals of North America appear to reflect long­ term climatic cycles, such as a drying from the Westphalian to the Stephanian, and a change of dominant vegetation from arborescent lycopods to tree-ferns. Abrupt changes in plant communities, as occur at the Cretaceous- Tertiary Boundary, have been used to support the idea of catastrophic events . Major changes in plant communities through time may also reflect important evolutionary innovations and the ability of plants to inhabit new environ­ ments, e . g . the evolution of leaves, the tree habit,

and the seed (see also Sections 1 . 8 .2, 1 . 10, 1 . 1 1 ; Collinson & Scott 1987) . Plant communities should not be considered in isolation. From the time of the earliest plant communities there is evidence of animal - plant in­ teractions (Section 1 .8 . 2) . Most involved arthro­ pods, at least until the Late Carboniferous when vertebrates first exploited plants as a major food source (Scott et al. 1 985) . From the Mesozoic and Tertiary comes diverse evidence for animal - plant interactions, the most significant being that between insects and flowering plants . This unique relation­ ship and the development of diverse pollination vectors was one of the main reasons for the success of angiosperms (Section 1 . 10) . Likewise there is a close link between the evolution of grasslands and vertebrate grazers in the Late Tertiary (Section 1 . 1 1 ; Friis et al. 1987) . Our knowledge of ancient plant communities is very limited but recent developments, especially in studies of plant taphonomy, will encourage rapid progress in this field .

References Broadhead, T.W. (ed . ) 1986 . Land plants. Notes for a short course. University of Tennessee, Department of Geological Sciences, Studies in Geology No. 15. Collinson, M.E. 1988. Freshwater macrophytes in palaeo­ limnology. Palaeogeography, Palaeociimatology, Palaeo­ ecology 62, 317-342. Collinson, M . E . & Scott, A . c . 1987. Factors controlling the organization and evolution of ancient plant communities . In: J . H.R. Gee & P.5. Giller (eds) Organizations of communities - past and present, pp . 399 -420 . British Ecological Society, Blackwell Scientific Publications, Oxford. Ferguson, D.K. 1985 . The origin of leaf-assemblages - new light on an old problem . Review of Palaeobotany and Palynology 46, 117- 188. Friis, E . M . , Chaloner, W . G . & Crane, P.R. (eds) 1987. The origin of angiosperms and their biological consequences. Cambridge University Press, Cambridge . Scheihing, M . H . & Pfefferkom, H.W. 1984. The taphonomy of land plants in the Orinoco delta: a model for the in­ terpretation of plant parts in clastic sediments of late Carboniferous age of Euramerica. Review of Palaeobotany and Palynology 41, 205 -240 . Scott, A . C . 1977. A review of the ecology of the Upper Carboniferous plant assemblages, with new data from Strathclyde . Palaeontology 20, 447-473. Scott, A . C . & Collinson, M . E . 1983 . Investigating fossil plant beds . Part 1 . Geology Teaching 7, 114- 122; Part 2, 8, 12-26. Scott, A . C . , Chaloner, W.G. & Paterson, S . 1985 . Evidence of pteridophyte- arthropod interactions in the fossil record .

4 . 1 1 Trace Fossils

355

plant fossil assemblages. Advances in Botanical Research 16, 95 - 1 9 1 .

Proceedings of the Royal Society of Edinburgh B86, 133- 140. Spicer, R . A . 1 989 . The formation and interpretation of

4 . 11 Trace Fossils S . G . P E M B E R T O N , R . W . FREY & T . D . A . S A U N D E R S

Trace fossils (or ichnofossils) are biologically pro­ duced sedimentary structures that include tracks, trails, burrows, borings, faecal pellets, and other traces made by organisms . Excluded are markings that do not reflect a behavioural function, such as those that result from the rolling or drifting of dead animals (Fig. 1 ) . Owing to their nature, trace fossils can be considered as both palaeontological and sedimentological entities, thereby bridging the gap between the two main subdisciplines in sedimentary geology . Recent summaries dealing with general ichnological principles can be found in publications by Frey (1975), Frey & Seilacher (1980), Ekdale et al. (1984), and Frey & Pemberton (1984, 1985) .

Classification of trace fossils Unique classification schemes have been developed in order to decipher, trace fossils because they represent behaviour rather than actual body remains . Historically, trace fossils have been classi­ fied in descriptive, preservational, taxonomic, and behavioural terms . Of these, the behavioural (or ethological) scheme is by far the most important; the behavioural record of benthic organisms is dic­ tated and modified by prevailing environmental parameters . Ekdale et al . (1984) recognized seven basic categor­ ies of behaviour: resting traces (cubichnia), loco­ motion traces (repichnia), dwelling structures

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356

4 Palaeoecology

(domichnia), grazing traces (pascichnia), feeding burrows (fodinichnia), farming systems (agrichnia), and escape traces (jugichnia) . Such fundamental behavioural patterns, although genetically con­ trolled, are not phylogenetically restricted. These basic ethological categories, for the most part, have persisted throughout the Phanerozoic. Individual tracemakers have evolved but basic behaviour essentially has not. For example, deposit feeders are preadapted to quiescent environments where deposited foodstuffs are most abundant, therefore they do not fare well in turbulent-water settings . The opposite is true of suspension feeders . Simi­ larly, locomotion traces can be preserved only under a strict set of environmental conditions . This ability to discern behavioural trends of benthic organisms represented in the rock record greatly facilitates environmental interpretations . The conceptual framework of ichnology

The importance of ichnology to the fields of strati­ graphy, palaeontology, and sedimentology stems from the following characteristics displayed by trace fossils : (1) long temporal range - which facilitates palaeontological comparisons of rocks differing in age; (2) narrow facies range - which reflects similar responses by organisms to given sets of palaeoeco­ logical parameters; (3) no secondary displacement trace fossils generally cannot be transported or reworked; (4) occurrence in otherwise unfossiliferous rocks - trace fossils are generally enhanced by diagenetic processes that destroy body fossils; and (5) creation by non-preservable soft-bodied biota many ichnofossils represent organisms that gener­ ally are not preserved because they lack hard parts; such organisms, in many environments, represent the greatest biomass . Significance of ichnology

Whether on local or regional scales, trace fossils are potentially capable of yielding substantial amounts of palaeontological, palaeoecological, and sedimen­ tological information (Table 1 ) . In general terms, the more significant kinds of information that can be gleaned from the ichnofauna include : (1) diversity, activity patterns, and the fossil record of 'non­ preservable' organisms; (2) spatial correlation and structural attitude of 'unfossiliferous rocks' ; (3) pro­ duction, alteration, and consolidation of sediment textures and fabrics; (4) facies and facies sequences; and (5) such intangibles as bathymetry (Section

4 . 1 9 .5), rates of deposition and erosion, oxygen levels (Section 4 . 19 . 4) , salinity (Section 4 . 19 . 3),

and substrate coherence and stability (Frey & Seilacher, 1980) . The ichnofacies concept

Perhaps the essence of trace fossil research involves the grouping of characteristic ichnofossils into recurring ichnofacies . This concept, developed by Adolf Seilacher in the nineteen-fifties and nineteen-sixties, was based originally on the fact that many of the parameters that control the distri­ bution of tracemakers tend to change progressively with increased water depth (Section 4. 19.5) . Nine recurring ichnofacies have been recognized, each named for a representative ichnogenus (Fig. 2) :

Scoyenia, Trypanites, Teredolites, Glossifungites, Psilonichnus, Skolithos, Cruziana, Zoophycos, and Nereites . These trace fossil associations reflect adap­ tations of tracemaking organisms to numerous environmental factors such as substrate consistency, food supply, hydrodynamic energy level, salinity, and oxygen levels (Frey & Pemberton 1984) . The traces in the non-marine assemblage (Scoyenia) are general and in need of revision; the marine softground ichnofacies (Psilonichnus, Skolithos, Cruziana, Zoophycos, and Nereites) are distributed according to numerous environmental parameters; the traces in the firmground (Glossifungites), wood­ ground (Teredolites), and hardground (Trypanites) ichnofacies are distributed on the basis of substrate type and consistency. Representative occurrences of the various ichno­ facies are summarized below . However, each may appear in other settings, as dictated by characteristic sets of recurrent environmental parameters . From the standpoint of ecological requirements of trace­ making organisms, for example, certain intertidal backbarrier environments are not all that different from certain subtidal forebarrier environments and may contain virtually identical suites of lebensspuren. The Scoyenia ichnofacies (Fig. 3) is a very gener­ alized association of trace fossils, found typically in continental red beds . However, prospects for the recognition of additional non-marine ichnofacies remain encouraging. For example, Ekdale et al. (1984) and Frey & Pemberton ( 1987) noted that distinct suites of trace fossils characterize aeolian dunes, fluvial overbank, palaeosol, and lake environments . The Psilonichnus ichnofacies (Fig . 4) is associated

357

4 . 1 1 Trace Fossils Table 1

Major contributions of ichnology to sedimentary geology. Relative importance (indicated by number of Xs) refers to the relative worth of that information in contemporary sedimentary geology. (After Frey & Seilacher 1980.) Geological setting Modem

Disciplines and components 1

2

3

4

5

Palaeontology (a) Fossil record of soft bodied animals (b) Patterns of activity by benthic organisms (c) Diversity of fossil assemblages (d) Evolution of metazoans and of behaviour

X XX XX X

Stratigraphy (a) Biostratigraphy of 'unfossiliferous' rocks (b) Correlation by marker beds (c) Structural attitude of beds (d) Structural deformation of sediments

Depositional environments and palaeoecology (a) Specific adaptations and behaviour of individual genera or species of organisms (b) Facies and facies successions (c) Bathymetry (d) Temperature and salinity (e) Depositional history (i) Rates of deposition (ii) Amounts of sediment deposited or eroded (f) Aeration of water and sediments (g) Substrate coherence and stability (h) Current direction

with supralittoral -upper littoral, moderate - low energy marine and/or aeolian conditions typically found in beach to backshore to dune environments . The trace fossils are characterized by: ( 1 ) vertical shafts, ranging from small structures, some with bulbous basal cells, to larger, irregularly J-, Y-, or U-shaped dwelling structures; (2) invertebrate and vertebrate crawling and foraging traces; (3) ver­ tebrate tracks and coprolites; (4) low density and diversity; (5) invertebrates - mostly predators or scavengers; and (6) vertebrates - mostly predators or herbivores .

XXX XXX XX XXX

XX X X X

Sedimentology (a) Production of sediment by boring organisms (b) Consolidation of sediment by suspension feeders (c) Alteration of grains by sediment-ingesting animals (d) Sediment reworking (i) Destruction of initial fabrics and sedimentary structures (ii) Construction of new fabrics and sedimentary structures

Consolidation of sediments (a) Initial history of lithification (b) Measures of compaction (c) Early diagenesis (d) Secondary mineralization

Ancient

XX XX X

X

X X

XXX XXX

XXX X X X

X XXX XXX XX

X X XX X X

XX XX XX XX X

XX X XX XX

The Skolithos ichnofacies (Fig. 5) is generally associated with high energy, sandy, shallow-marine environments . The trace fossils are characterized by: (1) predominantly vertical, cylindrical and U­ shaped burrows; (2) few horizontal structures; (3) few structures produced by mobile organisms; (4) low diversity, although individual forms may be abundant; and (5) mostly dwelling burrows con­ structed by suspension feeders . The Cruziana ichnofacies (Fig. 6) usually is associated with infralittoral- shallow circalittoral marine substrates below fairweather wave base and

4 Palaeoecology

358

G LD 5 5 1 FU N G I T E S

Fig. 2 Schematic diagram illustrating the general distribution of the nine recurring ichnofacies. The softground ichnofacies are generally distributed according to numerous ecological parameters which may be replicated in more than one environmental setting. For instance, the Skolithos ichnofacies is found not only in shallow, high energy substrates but also in offshore storm sands and submarine fans. Of the remaining ichnofacies three are substrate controlled, with the Trypanites ichnofacies in fully lithified substrates, the Glossifungites ichnofacies in semi-consolidated substrates, and the Teredolites ichnofacies in xylic substrates . These suites will occur wherever the requisite substrate is found; for example, the Glossifungites ichnofacies can be associated with exhumed muds in the shoreface or along the sides of submarine canyons .

2

Fig. 3 Trace fossil association considered to be indicative of the Scoyenia ichnofacies sensu stricto. 1 Scoyenia, 2 Ancorichnus, 3 Cruziana, including the 'Isopodichnus' of various authors, 4 Skolithos . (After Frey & Pemberton 1984, by permission from the Geological Association of Canada . )

Fig. 4 Trace fossil association characteristic of the Psilonichnus ichnofacies . 1 Psilonichnus, 2 Macanopsis.

above storm wave base . The trace fossils are charac­ terized by: (1) a mixed association of vertical, inclined, and horizontal structures; (2) presence of traces constructed by mobile organisms; (3) gener­ ally high diversity and abundance; and (4) mostly feeding and grazing structures constructed by deposit feeders .

The Zoophycos ichnofacies (Fig. 7) ideally is found in circalittoral-bathyal, quiet-water marine muds or muddy sands; below storm wave base to fairly deep water; in areas free of turbidity flows and subject to oxygen deficiencies . The trace fossils are characterized by: (1) low diversity, but individual traces may be abundant; (2) grazing and feeding

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359

4 . 1 1 Trace Fossils

Fig. 7 Restricted trace fossil association characteristic of the Zoophycos ichnofacies. 1 Phycosiphon, 2 Zoophycos, 3 Spirophyton . =

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Trace fossil association characteristic of the Skolithos ichnofacies . 1 Ophiomorpha, 2 Diplocraterion, 3 Skolithos, 4 Monocraterion . (After Frey & Pemberton 1984, by permission from the Geological Association of Canada. )

Fig. 5

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Fig. 8 Trace fossil association characteristic of the Nereites ichnofacies . 1 Spirorhaphe, 2 Urohelminthoida, 3 Lorenzinia, 4 Megagrapton, 5 Paleodictyon, 6 Nereites, 7 Cosmorhophe. (After Frey & Pemberton 1984, by permission from the Geological Association of Canada . ) =

=

=

=

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=

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Diverse trace fossil association characteristic o f the Cruziana ichnofacies . 1 Asteriacites, 2 Cruziana, 3 Rhizocorallium, 4 Aulichnites, 5 Thalassinoides, 6 Chondrites, 7 Teichichnus, 8 Arenicolites, 9 Rosselia, 10 Planolites. (After Frey & Pemberton 1984, by permission from the Geological Association of Canada.)

Fig. 6

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structures produced by deposit feeders; and (3) horizontal to gently inclined spreiten structures . The Nereites ichnofacies (Fig. 8 ) typically is associated with bathyal- abyssal, low energy, oxygenated marine environments subject to per­ iodic turbidity flows . The trace fossils are charac­ terized by: (1) high diversity but low abundance; (2) complex horizontal grazing traces and patterned feeding-dwelling structures; (3) numerous crawl­ ing-grazing traces and sinuous faecal castings; and (4) structures produced by deposit feeders, sca­ vengers, or harvesters . The remaining three ichnofacies are specialized, substrate-controlled and, environmentally, very

general in scope . The Glossifungites ichnofacies (Fig. 9) develops in firm but unlithified substrates (i. e . dewatered muds) . Such substrates can dewater a s a result of burial and are made available to trace­ makers if exhumed by later erosion. Exhumation can occur in shallow-water environments as a result of coastal erosion processes or from submarine channels cutting through previously deposited sediments. Such horizons may be critical in the evolving concept of sequence stratigraphy. The Trypanites ichnofacies (Fig. 10) characterizes fully lithified marine substrates such as hard­ grounds, reefs, rocky coasts, unconformities, and other kinds of omission surfaces . The Teredolites ichnofacies (Fig. 11), on the other hand, encompasses a characteristic assemblage of borings in marine xylic (woody) substrates . These differ from lithic substrates in three main ways: (1) they may be flexible instead of rigid; (2) they are composed of combustible material instead of mineral matter; and (3) they are readily biodegradable. Such differences indicate that the means by which, as well as the reason for which, these two types of substrates are

4 Palaeoecology

360

Trace fossil association characteristic of the Glossifzmgites ichnofacies . 1 = Thalassinoides or Spongeliomorpha, 2 Gastrochaenolites, 3 = Skolithos, 4 = Diplocraterion, 5 Psilonichnus . (After Frey & Pemberton 1984, by permission from the Geological Association of Canada . )

Fig. 9

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penetrated are different. Again, such assemblages will be of considerable importance in defining sequence and parasequence boundaries .

Trace fossil association characteristic of the Trypanites ichnofacies. 1 = echinoid grooves, 2 Rogerella, 3 = Entobia, 4= Trypanites, 5 = Gastrochaenolites, 6 = Trypanites, 7 = polychaete boring. (After Frey & Pemberton 1984; by permission from the Geological Association of Canada . ) Fig. 10

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Palaeobiological implications

Trace fossils record the activities of benthic organ­ isms, many of which are soft-bodied and are not readily preserved. This 'less preservable group' includes entire phyla (such as the nemerteans, nematodes, nematomorphs, annelids, sipunculans, echiurans, pogonophores, priapulans, phoronids, and enteropneusts) or classes (i . e . anthozoans, aplacophorans, holothuroids, and demosponges) . Many of these lineages are diverse (i. e . at present there are 18 000 extant species of annelids, 15 000 species of nematodes, 900 species of nemerteans, and 320 species of sipunculans) and many are known to have originated at the start of the Phanerozoic. For example, annelids, echiurans, pogonophores, priapulans, phoronids, and enteropneusts are known from deposits as old as Cambrian . Tra­ ditionally, however, palaeontologists have relegated such groups to 'minor phyla' status and have ignored them in: (1) the analysis of diversity trends through time (Sections 1 . 6, 2 . 7); (2) the taphonomic implications of the 'incomplete fossil record' (Sec­ tion 3 . 12); (3) the evolution of infaunal suspension and deposit feeders (Section 1 . 7 . 1 ) ; and (4) the interpretation of population strategies . Although the phylogenetic relationships o f trace fossils are difficult to establish, careful analysis of circumstantial evidence can yield convincing and important interpretations (Osgood in Frey 1975).

Trace fossil association characteristic o f the Teredolites ichnofacies, dominated by Teredolites . (After Bromley et al . in Miller et al. 1984.) Fig. 11

Palaeoecology and environmental reconstructions

The concept of functional morphology, a basic premise employed by ecologists and palaeo­ ecologists in environmental reconstructions, is equally applicable to ichnology . In fact, ichnofossils are unique in that they represent not only the morphology and ethology of the tracemaking or­ ganism but also the physical characteristics of the substrate; they are closely linked to the environ­ mental conditions prevailing at the time of their construction . Frey & Seilacher (1980) re-emphasized that such variables as bathymetry, temperature and

4 . 1 1 Trace Fossils salinity (Section 4 . 19), rates of sediment deposition, amounts of sediment deposited or eroded, aeration of water and sediment, and substrate coherence and stability have a profound effect on resultant ichno­ fossil morphologies and hence can be used in the determination of original biological, ethological, and sedimentological conditions . Rhoads (in Frey 1975) stated that one of the most important variables controlling the distribution of bottom-dwelling or­ ganisms is the nature of the substratum, such as grain-size distribution, organic content, bottom compaction, and sedimentation rate . In lithified deposits, sediment grain size and organic content are directly observable; however, bottom hardness and sedimentation rate can best be approximated using trace fossils (Rhoads in Frey, 1975) . Size or composition of sediment grains in many instances is less important than the geotechnical properties of the substrate . Details of the palaeoecological sig­ nificance of trace fossils were summarized in publi­ cations by Frey (1975), Ekdale et al . (1984), Ekdale (1985), and Frey & Pemberton (1985) . The application of ichnology to palaeoenviron­ mental analysis goes far beyond the mere establish­ ment of gross or archetypal ichnofacies . For instance, shallow-water, coastal marine environ­ ments comprise a multitude of sedimentological regimes, which are subject to large fluctuations in many physical parameters . In order to fully com­ prehend the depositional history of such zones in the rock record, it is imperative to have some reliable means of differentiating subtle changes in these physical characteristics . Detailed investigations of many of these coastal marine zones in Georgia have shown the value of utilizing biogenic sedimentary structures (in concert with physical sedimentary structures) in delineating them (Frey & Pemberton 1987) . The application of these studies in de­ ciphering palaeoenvironments has also proved sig­ nificant (Miller et al . 1984; Curran 1 985) . Similarly, the use of ichnofossils in the interpret­ ation of freshwater deposits is becoming increas­ ingly important. Reviews by Chamberlain (in Frey 1975) and Ekdale et al. (1984) stressed the abundance and diversity of tracemaking organisms in fresh­ water environments and emphasized their potential importance in palaeoenvironmental reconstruc­ tions . Distinct differences in ichnofossil types and abundance have been reported from a wide range of freshwater- terrestrial environments, in both ancient and recent settings (Ekdale et al. 1984) . Recently, marginal marine environments (includ­ ing tidal channels, estuaries, bays, shallow lagoons,

361

and delta plains) have been recognized with more frequency in the rock record . Such environments characteristically display steep salinity gradi­ ents which, when combined with corresponding changes in temperature, turbulence, and oxygen content, result in a physiologically stressful en­ vironment for numerous groups of organisms . The typical trace fossil suite in such environments reflects these stresses and is characterized by: (1) low diversity; (2) ichnotaxa which represent an impoverished marine assemblage rather than a true mixture of marine and freshwater forms; (3) a domi­ nance of morphologically simple structures con­ structed by trophic generalists; and (4) a mixture of elements which are common to both the Skolithos and Cruziana ichnofacies . One of ichnology's greatest strengths, the bridg­ ing of sedimentology and palaeontology, in some ways can be its greatest liability. Sedimentologists tend to use a strict uniformitarian approach to palaeoenvironmental interpretation and rely heavily on modern analogues . Palaeontologists, on the other hand, must temper their observations in the light of organic evolution. Although trace fossils can be considered as biogenic sedimentary structures and are difficult to classify phylogenetically, they are constructed by biological entities and are thus sub­ jected to evolutionary trends . For example, occur­ rences of well developed terrestrial trace fossil assemblages are much more prevalent in post­ Palaeocene rocks. This development corresponds to the evolutionary explosion of the insects brought on by the diversification of the angiosperms in the Late Cretaceous (Section 1 . 10) . Prior to this time terrestrial substrates may not have been as exten­ sively bioturbated due to a paucity of tracemakers . Likewise, patterned grazing traces, which charac­ terize deep-sea sediments, show a trend toward fuller organization through most of the Phanerozoic. This trend may be related to the evolution of more efficient foraging strategies (Frey & Seilacher 1980) . For these reasons, palaeoenvironmental interpretations based on trace fossils must be con­ sidered not in strict uniformitarian terms, but rather, in actualistic ones . Equally important, unique, quantitative environ­ mental indicators are indeed rare in the geological record, and ichnology is no exception (Frey & Seilacher 1980) . However, trace fossils can supply a wealth of environmental information that cannot be obtained in any other way and which should not be ignored . Their potential usefulness is accentuated when fully integrated with other (chemical, physi-

4 Palaeoecology

362

cal, and ethological) lines of evidence . Combined studies of physical and biogenic sedimentary struc­ tures constitute a powerful approach to facies analysis .

References Curran, H.A. (ed . ) 1985 . Biogenic structures: their use in interpreting depositional environments . Special Pub­ lication of the Society of Economic Paleontologists and Mineralogists, No. 35 . Ekdale, A.A. 1985 . Paleoecology of the marine endobenthos . Palaeogeography, PalaeoC/imatology, Palaeoecology 50, 63- 81 . Ekdale, A . A . , Bromley, R . C . & Pemberton, S . C . 1984. Ichnology: trace fossils in sedimentology and stratigraphy. Society of Economic Pale ontologists and Mineralogists, Short Course Notes, No. 15.

Frey, R.W. (ed . ) 1975 . The study of trace fossils . Springer­ Verlag, New York. Frey, R.W. & Pemberton, S . C . 1984. Trace fossil facies models . In: R.C. Walker (ed . ) Facies models (2nd edn), pp. 1 89 207. Ceoscience Canada, Reprint Series, No . 1 . Frey, R . W . & Pemberton, S . C . 1985 . Biogenic structures in outcrops and cores. 1 . Approaches to ichnology. Bulletin of Canadian Petroleum Geology 33, 72 - 1 15 . Frey, R . W . & Pemberton, S . C . 1987. The Psilonichnus ichnocoenose and its relationship to adjacent marine and nonmarine ichnocoenoses along the Ceorgia coast. Bul­ letin of Canadian Petroleum Geology 35, 333- 357. Frey, R.W. & Seilacher, A . 1980. Uniformity in marine inver­ tebrate ichnology. Lethaia 13, 1 83-207. Miller, M . F . , Ekdale, A.A. & Picard, M.D. (eds) 1984. Trace fossils and paleoenvironments: marine carbonate, mar­ ginal marine terrigenous and continental terrigenous set­ tings . Journal of Paleontology 58, 283-597.

4 . 12 Evidence for Diet J . E . P O L L A RD

Introduction

The diet of ancient organisms may be deduced from a variety of direct and indirect evidence from body fossils and trace fossils. Direct evidence comes from the discovery of ingested prey in a predator's skel­ eton and the analysis of gut contents or coprolites (fossil faeces) . Regurgitates or rejected prey with bite marks indicating predation, or trace fossils reflecting grazing, rasping, or highly patterned feed­ ing activity, are major categories of indirect evi­ dence . More generalized information on diet may be derived from functional analysis of specialized feeding organs, such as appendages in arthropods, radulae in gastropods or cephalopods, and teeth and jaws in vertebrates . Such structures are usually interpreted by analogy with living animals, e . g . the use of modern dental analogues to deduce the diet of fossil mammals . Feeding habits - general type of diet

Many fossil invertebrates show adaptation of their

hard parts to specialized feeding - either as primary consumers of suspended or benthic detritus, or as carnivores (usually predators; see also Section 4 . 1 3) . Arthropods lacking grasping or feeding append­ ages, such as trilobites, are interpreted as detritus feeders, producing the furrow feeding traces Cruziana. However, some trilobites, like Olenoides in the Cambrian Burgess Shale, may have used leg spines to tear soft-bodied prey. Carnivorous arthro­ pods frequently possess specialized grasping, tearing, or crushing appendages, whether active predators like Sidneyia from the Burgess Shale (Conway Morris 1986) or scavenging decapod crustaceans, probably crabs, which cut open body chambers of eleganticeratid ammonites as they lay on their sides on the Jurassic sea floor (Lehmann 1981) . The gastropod radula has been used by patel­ liform types in algal grazing on hard substrates at least since the Cretaceous, and by carnivorous forms to bore into bivalve shells (Bishop 1975) . Most vertebrates have toothed jaws. The shape of the tooth is closely related to its function or to the type of food it must prepare for digestion . In general

4 . 1 2 Evidence for Diet terms, piercing teeth are cone shaped; shearing or cutting teeth are long and blade like; crushing teeth are low, flat and button shaped; grinding teeth often have complex cusping patterns and a con­ tinuous growth or replacement mechanism. The arrangement of teeth types in the jaw is also an indication of diet. Although correlation of dentition and diet is best known among mammals, it also provides major in sights into the feeding habits and diet of fossil sharks and marine and terrestrial reptiles of the Late Palaeozoic and Mesozoic eras . Nectic hunting sharks (e . g . Carcharodon megalodon, Miocene) pos­ sess the familiar triangular sharks' tooth, while benthic sharks and rays (e . g . Ptychodus, Cretaceous) feeding on shelled invertebrates have button­ shaped crushing teeth. Marine reptiles have diverse specialized dentitions which can sometimes be related to diet, as indicated by gastric contents or bite marks on prey. The placodonts of Permian seas were highly specialized predators on shelled inver­ tebrates, with anterior chisel-like nipping teeth and flat crushing teeth in the rear of the jaws and on the palate (Fig. 1) . Permian bivalves are known with crescentic chips removed from the edge of the shell, perhaps resulting from such predation (Bishop 1975) . Selective diets among Jurassic ichthyosaurs are reflected by the piercing teeth in fish-eating forms and the loss of teeth in late Jurassic cepha­ lopod eating ophthalmosaurs . These diets are con­ firmed by gastric contents (see below) . Similar dietary preferences can also be recognized among Jurassic plesiosaurs; these predators retained their teeth, specializing as small headed, long necked fish-eating 'plesiosaurids' and large headed, short necked 'pliosaurids' which ate other marine reptiles and cephalopods (Norman 1985) . These diets are confirmed by stomach contents, which usually con­ tain gastroliths (stomach stones) to aid the digestive breakdown of prey. In the Late Cretaceous the marine predaceous mososaurs developed several dietary specializations : fish eaters can be recognized from stomach contents; cephalopod eaters even preyed on ammonites, as indicated by specimens of the Cretaceous Pachydiscus bitten up to 16 times (Bishop 1975); a probable shellfish eater (Globidens) possessed rather flattened placodont-like teeth. Dinosaurs show a remarkable range of dietary specializations (Norman 1985) . Carnivorous dino­ saurs include coelurosaurs with small, sharply pointed teeth and weak jaw mechanics, ornithomi­ mosaurs which lacked teeth, and large carnosaurs with tearing claws and serrated dagger-like teeth .

363

Fig. 1 Skull of a placodont reptile (Placodus) with anterior nipping teeth, and cheek and palatal crushing teeth, suggesting that the animal fed on shelled invertebrates, probably brachiopods or bivalves. Original skull about 0.25 m long . (After Bishop 1975 . )

Stomach contents of coelurosaurs (Coelophysis, Triassic) show that some were cannibalistic on their own young, while others (e . g . Compsognathus, Jurassic of Solnhofen) were fast, agile hunters, preying on contemporary running ground lizards (Bavarisaurus) . There has been considerable debate about the diet of the toothless ornithomimosaurs, including suggestions that they were insectivorous, shrimp eaters, frugivores, or omnivores . Bite marks preserved on large Jurassic sauropod vertebrae cor­ respond with the size and spacing of the teeth of Allosaurus, a contemporary carnosaur. A fish-eating diet has been suggested for the carnivorous dino­ saur Baryonyx, recently discovered in the Cretaceous rocks of Surrey, on account of its elongate jaws with numerous teeth and scales of Lepidotes preserved within the rib cage . Dentition and jaw mechanisms indicate two dis­ tinct feeding habits among herbivorous dinosaurs . Those with unspecialized chisel or peg shaped teeth, such as sauropods, stegosaurs, and ankylosaurs, are believed to have simply stripped off vegetation, which was swallowed whole into a capacious stomach where it was pounded by gastroliths and

364

4 Palaeoecology

slowly digested, as shown by preserved stomach residues . Iguanodonts, hadrosaurs, and ceratopsian dinosaurs had a horny beak at the front of the mouth and a battery of grinding teeth at the rear. These teeth were continually replaced and, although the jaws were capable only of up and down move­ ment, the tooth battery produced a very efficient oblique mill to grind up food prior to swallowing. Gastric contents of late Cretaceous 'mummified' hadrosaurs in western Canada contain conifer needles, twigs, and seeds, as well as angiosperm fragments, but lacked gastroliths . This supports the suggestion that these dominant Cretaceous her­ bivores had evolved a feeding mechanism capable of coping with a diet of tough conifers and angio­ sperms, rather than the softer vegetation of Bennettitales, cycads, or seed ferns exploited in the Jurassic sauropod-stegosaur type of feeding. Ingestion - digestion of food regurgitates and gastric re si dues

The most direct evidence for diet is where food remains are preserved within the body of the host before becoming unrecognizable through the diges­ tive process . Such remains are often termed pre­ coprolite and may be preserved as regurgitates, gut contents, gastric contents, or intestinal residues. Regurgitates, which differ from gut contents in being preserved remote from the producer, and from coprolites in lacking a phosphatic matrix, are an important source of dietary information. Modem birds regurgitate pellets which are very distinctive as to producer and so to predator -prey relation­ ships (Bishop 1975) . Fossil regurgitates composed of bivalve shell debris (Myalina), probably produced by sharks, have been recognized in Carboniferous shales, and in Cretaceous carbonates composed of shell debris of Inoceramus (bivalve) or claws of the crustacean Callianassa (Bishop 1975) . Regurgitates can be dispersed by currents during sedimentation and so may introduce an unrecognized bias into the fossil record . In the Middle Cambrian Burgess Shale (Section 3 . 1 1 . 2), gut contents are known from several animals, both predators at the top of the food chain and some infaunal deposit feeders, the primary con­ sumers . The predatory arthropod Sidneyia fre­ quently has gut contents composed of ostracodes, small trilobites, hyolithids, and fragmented inarticulate brachiopods . Another predator on hyolithids and inarticulate brachiopods was the priapulid worm Ottoia, which swallowed its prey

whole and at times was cannibalistic. The annelid worm Burgessochaeta has gut contents of sediment, sometimes formed into faecal pellets, suggesting that it was an infaunal deposit feeder. This evidence of diet from gastric contents and its correlation with functional morphology (see above) has enabled the trophic web of the Burgess Shale community to be reconstructed in considerable detail (Conway Morris 1986; Section 4. 16) . Gut contents are also important in the analysis of plant- arthropod relationships in Carboniferous coal swamps. Specimens of the large myriapod Arthropleura armata with gut contents of lycopod wood, and of an early insect with abundant spores in the gut, demonstrate the development of a phyto­ phagous diet among arthropods by the Late Carbon­ iferous. This is further supported by coprolites from coal balls (see below) . Several Jurassic Lagerstatten in Europe preserve gastric residues which shed light on the diets of ammonites . Liassic ammonites Arnioceras and Hildoceras are preserved with gastric remains of foraminifera, ostracods, and the jaws of juvenile ammonites in their body chambers . A specimen of Physoderoceras has gastric contents composed of arm and calyx fragments of the free swimming crinoid Saccocoma, which is also a major component of the coprolite Lumbricaria from the contempor­ aneous Solnhofen Limestone (Section 3 . 1 1 . 7) . Such evidence suggested to Lehmann (1981) that ammo­ nites may have been benthic scavengers rather than active predators . Several predatory fish have been fossilized with their prey only partly swallowed, e . g . Caturus in the Solnhofen Limestone (Jurassic) and a perch (Mioplosus) partly ingesting a herring (Knightia) from the Eocene Green River Formation of Wyoming (see p . 305; Bishop 1975) . Occasionally, gastric contents are sufficiently well preserved to enable detailed analyses of diet, feed­ ing habits, and the trophic web among the ver­ tebrate fauna to be established . A hybodont shark from the Jurassic Posidonia Shale of Holzmaden, West Germany (Section 3 . 1 1 . 6 ) , has a mass of over 100 belemnite rostra preserved between its pectoral fins (Fig . 2) . Ichthyosaurs from the same formation mostly have dibranchiate cephalopod hooklets in their stomach contents, although fish remains (Dapedius, Leptolepis, Ptycholepis, and Pachycomus) also occur and a complex food web has been estab­ lished. Lower Liassic shales at Lyme Regis have also produced some remarkable specimens . One young ichthyosaur found in the nineteen-sixties

4 . 1 2 Evidence for Diet

365

Fig. 2 Dorso-ventrally compressed skeleton and body outline of hybodont shark Hybodus with gastric residue of many belemnite rostra preserved between its pectoral fins. Posidonia Shales, Lower Jurassic; Holzmaden, West Germany. Original specimen about 2 m long . (From Stuttgart Museum fur Naturkunde . )

has a gastric mass of cephalopod hooklets (estimated at 478 000 ± 53%) representing a consumption of between 760 and 2430 individual cephalopods (Pollard 1968) . This estimate compares closely with the remains of between 2000 and 14 000 squids recovered from the stomachs of recent sperm whales (Pollard 1968) . Although these cephalopod hooklets appear to belong to belemnites, the rostra are absent, unlike in the hybodont shark from Holzmaden (Fig. 2) . It appears that only the head and arms of these belemnites were swallowed after the body with rostrum had been bitten off and regurgitated . The Eocene oil shale deposit of Grube Messel, West Germany (Section 3 . 1 1 . 8) has yielded some remarkable stomach contents of mammals, includ­ ing bats and early horses . The bats fed on nocturnal Lepidoptera and therefore suggest that these aerial predators had developed an ultrasonic location system as far back as Eocene times . The early horse Palaeotherium has gastric contents of leaves and fruit, proving that it browsed on forest vegetation (as inferred from dentition 70 years ago), and thus had quite a different diet from more recent grass eating horses . Pollen analyses of the gastric contents of late Pleistocene Siberian mammoths show that they fed mostly on grass . The state of ripeness of the

grass seeds indicate that the mammoths usually died at the beginning of the summer. The complete pollen spectra from these gastric contents show that they inhabited steppes and open tundra with a warmer climate than Siberia today.

Defecated food remains faecal pellets and coprolites

Careful analysis of size and form, macroscopic con­ tents, microfauna and microflora, mineralogy, and geochemistry of coprolites has provided dietary information on organisms ranging from Palaeozoic terrestrial invertebrates to prehistoric man. Faecal material produced by invertebrates is usually in the form of discrete pellets (microcopro­ lites) or more rarely strings, representing unbroken discharge . Faecal pellets vary greatly in size, form, composition, and nature of the invertebrate pro­ ducer (see Moore in Hantzschel et al. 1968), but two broad categories are of particular interest in the fossil record : those of early terrestrial herbivores and marine substrate feeders . Burrows in a late Ordovician palaeosol in Pennsylvania are packed with ferruginous faecal pellets believed to have been produced by the earliest known terrestrial

366

4 Palaeoecology

arthropods . Coprolites from the Upper Carbonifer­ ous shales and coal-balls contain lycopod cuticle remains and spores. Distinct size groupings of these coprolites suggest that they were possibly produced by soil mites (30 - 60 !-lm), Collembola (100- 700 !-lm) and millipedes (greater than 1 mm) . Borings in Pennsylvanian fern sterns or cordaitean wood are packed with coprolites, while coprolites containing undigested fragments of leaf cuticle have been found associated with Glossopteris leaves with insect eaten edges in Carbo-Perrnian deposits in India. Such coprolite evidence suggests that detritus feed­ ing soil arthropods existed as early as the Late Ordovician, and that diverse feeding mechanisms and diets had developed among phytophagous arthropods by Late Palaeozoic times . Faecal pellets produced by substrate feeding invertebrates frequently have distinctive shapes or occur in association with particular burrows or trails . Strings o f sausage-like faecal pellets, Tomaculum, are common in both Ordovician and Westphalian marine shales; in Mesozoic carbonate sediments, burrows like Rhizocorallium (Muschelkalk, Triassic) or Thalassinoides (Great Oolite, Jurassic) are fre­ quently stuffed with pellets . The faecal pellets in thalassinoid systems are often the distinctive form Favreina with ten internal, crescent-shaped longi­ tudinal canals, and were probably produced by deposit feeding shrimps like Eryon or Glyphaea, which inhabited the burrow systems . Most vertebrate coprolites are composed of calcium phosphate or more rarely organic matter, and are frequently replaced by siderite, limonite, or silica during diagenesis (Hantzschel et al. 1968) . They were produced predominantly by carnivorous predators, but the great variety of size and shape (and an insufficient knowledge base for the faeces of recent animals) makes assignment to specific producers difficult. Spiral coprolites (Fig. 3) fre­ quently possess delicate surface markings believed to result from the intestinal membranes of their producers . They have been regarded therefore as infillings of spiral intestines (enterospirae; Fig. 3) rather than defecated coprolites . However, recent observations on living sharks has shown that the spiral form can be retained on discharge into the colon from the spiral intestine, so that they are probably truly cololitic-coprolitic in origin. These distinctive coprolites were produced by a range of fish groups with spiral intestinal valves, including agnathans, actinopterygians, dipnoans, and coela­ canths (Fig. 3G, H, Macropoma mantelli, Chalk, Up­ per Cretaceous) . Most commonly, however, they

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were probably produced by chrondrichthyans, sharks, or rays (Fig. 3A - F) . Coprolites from Cretaceous non-marine sedi­ ments are frequently assigned to terrestrial reptile producers, often dinosaurs or crocodilians . The abundant phosphatic coprolites found in the Wealden sediments at Bernissart, Belgium, associ­ ated with Iguanodon skeletons, were at first assigned

4 . 1 2 Evidence for Diet to that dinosaur (Bertrand in Hantzschel et al. 1968) . However, their phosphatic nature and content of vertebrate bones suggests that the producer was a predator, not a browsing herbivore like Iguanodon (Norman 1985) and the associated crocodiles seem more likely producers (see Bertrand; Abel; Casier; all in Hantzschel et al . 1968) . Although some very large coprolites (up to 0 . 29 m long) may have a dinosaur origin, as yet no undoubted coprolites of herbivorous dinosaurs have been described . By con­ trast, crocodile coprolites are frequently recognized and analysed, especially from Late Cretaceous and Eocene non-marine sediments of North America. Two broad diets seem to be represented, piscivorous forms which fed on the Gar Pike Lepisosteus and more omnivorous forms which defecated fish bones, reptile scales, seeds, and leaves of plants (especially the water plant Salvinia) . Pollen analysed from phos­ phatic coprolites appears to have been ingested with drinking water or silt swallowed while scavenging, and it reveals more information about the habitat of the producer than the diet. Although mammal coprolites occur fairly widely in Cenozoic sediments, those of Pleistocene or post­ glacial mammals have received most attention. In his classic work on Pleistocene cave deposits Buckland (1823) described an unusual substance 'album graecum' from cave earths associated with mammal bones. He identified this as being the coprolite of cave hyaenas, composed of digested bone and complementary to the dietary evidence provided by fragmented mammal bones with hyaena tooth marks in the same deposits . Sub­ sequent workers have recognized coprolites produced by rodents, cave bears, and other mammals in Pleistocene cave deposits (Hantzschel

et al. 1968) . Desiccated coprolites of both Late Pleistocene ground sloths and prehistoric humans in North America have yielded much detailed information on diet and contemporary environments . Coprolites from cave shelters in New Mexico and Arizona

367

(dated as 40 000 - 1 1 000 BP) show that ground sloths fed on a vegetation of juniper woodlands and mon­ tane conifers, which still persist in the area today. Assessments of the energy, fibre, and nutrient values of the diet of these ground sloths has failed to explain their extinction (at about 11 000 BP) as a result of climatic change or dietary stress; human predation remains a likely cause . Coprolites have been used for the past two decades as a means of determining ancient human diet. For example, they showed that the diet of the inhabitants of Tamaulipas, Mexico (7000 - 1700 BC), was largely vegetarian, but also included mice, snakes, lizards, grasshoppers, and perhaps other insects; and that the diet of ancient inhabitants of Peru (2500 - 1200 BC) was entirely vegetarian (Callen in Hantzschel

et al. 1968) .

References Bishop, G . A . 1975 . Traces of predation. In: R.W. Frey (ed .) The study of trace fossils, pp. 261 -281 . Springer-Verlag, New York. Buckland, W. 1823 . Reliquiae diluvianae. Murray, London . Buckland, W. 1836 . Geology and mineralogy considered with reference to natural theology. Vols 1 & 2. The Bridgewater Treatise. William Pickering, London . Conway Morris, S . 1986. The community structure of the Middle Cambrian Phyllopod Bed (Burgess Shale). Palaeontology 29, 423-467. Franzen, J . L . 1985 . Exceptional preservation of Eocene ver­ tebrates in the lake deposit of Grube Messel (West Germany) . Philosophical Transactions of the Royal Society of London B311, 181 - 186. Hantzschel, W., El-Baz, F. & Amstutz, G . c . 1968. Coprolites: an annotated bibliography. Memoir of the Geological Society of America, No. 108. Lehmann, U. 1981 . The ammonites: their life and their world. Cambridge University Press, Cambridge. Norman, D . 1985 . The illustrated encyclopaedia of dinosaurs . Salamander Books, London . Pollard, J . E . 1968. The gastric contents of an ichthyosaur from the Lower Lias of Lyme Regis, Dorset. Palaeontology 11, 376 -388.

4 . 13 Predation

4 . 1 3 . 1 Marine

upon the prey skeleton. In the process of insertion and extraction, the predator penetrates the skeleton

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of the prey and removes flesh through the aperture, again without damaging the skeleton. These modes of predation are not generally reflected in the hard part morphology of predators and thus are not identifiable in the fossil record . Some predators kill their victims by grasping them and transporting them into environments in which they cannot sur­ vive, e . g . in the case of shore birds which commonly transport marine molluscs into subaerial environ­ ments where they feed upon them. The chances of detecting this mode of predation in the fossil record are slim. Preingestive breakage and drilling both leave direct trace fossil evidence in the form of bite or crush marks and circular to parabolic bore holes. Both of these modes of predation have been the subject of several recent studies (for reviews see Vermeij 1987) . Many predators break or puncture the shells of their victims prior to ingestion, using a variety of tools. Several marine molluscs employ a form of forced entry to break or separate the valves or plates of their prey. For example, the gastropod Acanthina utilizes a sharp spine on its shell's outer lip to break apart the plates of barnacles; whelks of the genus Busycon use the sharp outer lip of their shell to chip and pry at the valve margins of bivalves . Cephalopods also possess chitinous or calcified beaks for biting or crushing prey. A wide variety of marine vertebrates, both living and fossil, utilize blunt pavement teeth to crush hard-shelled prey; these include rays, ptyctodonts, placodonts, and various marine sharks . Most sharks, as well as fossil mosasaurs, use sharp teeth to pierce or fracture the shells of their prey. In the process, they may leave distinctive bite marks, such as divots or rows of holes in those shells (Fig. lA-D) . Crustaceans use three distinct strategies to break the shells of their prey, and in the process also produce distinctive traces . The shells may be crushed between the op­ posed surfaces of claws . Peeling involves the piece by piece breakage of the outer margin of gastropod shells by crabs (Fig . 1C) until the flesh of the organ­ ism becomes accessible to the predator. Still other crustaceans, primarily stomatopods, crush the shells of their prey by pounding them with blunt, ex­ panded segments of their maxillipeds .

Introduction

Predation, the killing and consumption of animals for food, is of fundamental importance in controlling diversity and abundance of organisms in modern marine environments . Predation was probably also critical in shaping longer term trends in adaptation; Vermeij (1977, 1987) has documented an evolution­ ary 'arms race' between marine shelled organisms and their predators through Phanerozoic time . Co­ evolution between organisms and their predators has led to an intensification of the struggle for existence and increased complexity of organisms through time, which Vermeij refers to as escalation . Predators form the apex of the biomass pyramid in any given community, and are commonly desig­ nated as first, second, or third order, depending on whether they feed primarily on herbivores or on other carnivores . Predator- prey interactions are normally con­ sidered to represent dependent coactions, and a considerable theory has been developed based on the assumption that population sizes of predator and prey are mutually dependent. Indeed, certain terrestrial community studies appear to document a dependency of predators on specific prey . However, it has also been argued that much predation, par­ ticularly amongst marine organisms, is of a non­ specific and opportunistic nature . In this case, the impact of predation on a particular prey species, and vice versa, may be less significant. Modes of predation

The act of predation involves several phases (Bishop 1975) : search, capture, penetration, ingestion, digestion, and defecation . The penetration and ingestion phases can be combined under the heading of sub­ jugation . Vermeij (1987) further subdivided the modes of subjugation employed by durophagous marine predators into five categories . Whole animal ingestion involves swallowing the entire body of the prey animal and generally leaves no distinct marks

368

369

4 . 1 3 Predation

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Fig. 1 Fossil evidence of predation. A, Cretaceous ammonite Placenticeras displaying rows of punctures apparently made by the teeth of a mosasaur, X 0.6. B, Recent gastropod shell exhibiting peeling damage inflicted by the predatory crab Calappa, x 1 . C , Devonian gastropod Palaeozygopleura with a healed, scalloped fracture o f the outer lip, probably resulting from a failed attempt at lip-peeling by a predator, x 5. D, Permian bivalve with crescentic breakage along valve margin, probably the result of fish predation, x 1 . E, Diagram showing locations of most frequent drilling on Recent bivalves from the Nile Delta; note selective positioning of boreholes near umbo. F, Diagram illustrating positions of complete (black) and incomplete (white) boreholes in the Devonian brachiopod Rhipidomella; note concentration near umbo. G- I, Recent gastropod boreholes in bivalve shells. G, complete borehole of Natica severa; note bevelled outer edge and change from circular (outer) to elliptical openings, x 6. H, incomplete borehole of Polinices duplicatus; note presence of raised boss at centre of view, x 6. I, boring of Murex fulvescens on the commissure of a bivalve shell, x 6. Figures redrawn from photographs as follows : A, Kauffman & Kesling 1960; B, Bishop 1975; C, Brett & Cottrell 1982; D, Boyd & Newell 1972; E, Reyment 1971 ; F, Smith et al . 1985; G - I, after Carriker & Yochelson 1968.

Drilling is a specialized mode of predation, largely restricted to marine molluscs, including both gastro­ pods andcephalopods . These organisms leave very distinctive drilling traces, referred to the ichnogenus Oichnus (Fig . IG- I), that provide direct records of successful predation. The boring procedure involves secretion of unknown acids by an accessory boring

organ and mechanical abrasion by the denticles of the radula. The entire process is relatively slow, requiring from 5 to 100 hours for completion. Conse­ quently, normally only a single hole is drilled per shell, although rarely one or more incomplete holes may be observed and there are instances of holes being produced in unoccupied shells. As a whole,

370

4 PaZaeoecoZogy

gastropod predatory boreholes can be distinguished from other types of borings in that they are circular in outline, penetrate the prey shell perpendicular to the shell, are parabolic or cylindrical in cross-section, and normally range from about 0 . 5 mm to 3 . 0 mm in diameter. Hole size is generally related to the size of the gastropod predator. Modern drilling gastropods are rather highly prey selective, favouring certain species of bivalves . They also show preferential positioning of the bore hole, most commonly near the centre of the prey shell (Fig. lE, F) . However, some Polynices and many muricids actually drill shells along the commissure (Fig. 11) . Naticid drill holes tend to be regularly parabolic in cross-section and, when incomplete, display a raised boss in the centre of the floor (Fig. 1H) . Muricid gastropods, on the other hand, produce holes that are cylindrical in outline, tend to be more randomly distributed on the shells, and do not show a raised boss when incomplete . A third group of gastropods, the cassids (helmet shells), produce circular holes in echinoid tests . Cephalopods drill primarily for the purpose of paralysing their prey. The hole is generally oblique to the shell surface and tends to be conical, but is rather irregular in size and shape. Cephalopod bore­ holes are not yet known from the fossil record . Fossil record of predation

Direct records of ancient predation are relatively rare in the fossil record; as Bishop (1975) noted, the evidence of predation is normally destroyed (liter­ ally eaten) in the process of its formation. However, several lines of evidence provide some insight into the evolutionary history of predation. The body fossil record of potential predators provides infor­ mation on the general ranges of different carnivor­ ous organisms. The predatory behaviour of fossil organisms may be inferred indirectly from morpho­ logical comparisons with living analogues known to have carnivorous habits, e . g . cephalopods and naticid gastropods . The fossil record commonly provides direct indications of a predaceous mode of life because the organs used in manipulation, biting, and ingestion of prey are typically heavily skeletonized and thus preservable . Such tools in­ clude the crushing claws of crustaceans, modified chelicerae of eurypterids, and a wide array of pave­ ment and biting teeth in vertebrate groups . Cephalopods with probable chitinous beaks are abundant from the Late Cambrian or Early Ordovician onward, but the direct fossil record of

calcified beaks (rhyncholites) does not begin until the Late Palaeozoic. Durophagous arthropods include mainly phyllocarids and eurypterids in the Palaeozoic; these had appeared by the Late Ordovician but attained maximum diversity in about the Middle Devonian. The decapod crustaceans in the Triassic evolved more efficient mechanisms of shell crushing by claws or maxillipeds. In the Jurassic, new groups of shell-crushing crustaceans evolved, including the stomatopods and brachyuran crabs. A major increase in durophagous predators involved the abrupt appearance of varied jawed fishes in the Devonian Period, including the piaco­ derms, ptyctodonts, hybodonts, and others (Fig. 2) . Certain sharks, such as Helodus, with shell-crushing pavement teeth, have been implicated by Alexander (1981) as producers of distinct crush marks in Carboniferous brachiopods. The large marine predators of the Mesozoic were dominated by reptiles within the subclass Diapsida: the placodonts (Placodontia), nothosaurs and plesio­ saurs (Sauropterygia), ichthyosaurs (Ichthyosauria), mosasaurs (Squamata; family Mosasauridae), and marine crocodiles (Crocodilia; family Metriorhyn­ chidae, Teleosauridae) . The evolution of large marine predator communities in the Mesozoic can be divided into four main periods of stability and slow diversification, separated by periods of re­ organization or extinction (Massare 1987, 1988) . Sharks and large fish continued to diversify through the Late Cretaceous, and were the impor­ tant marine predators in the Early Tertiary. Sharks probably reached their peak with the giants of the Miocene . Whales appeared in the Eocene, but early forms, the zuglodonts, were heterodont, long­ bodied ambush predators more similar in body form to the Cretaceous mosasaurs than to modern whales. Seals, sea-lions, and modern whales appeared in the Late Oligocene and Miocene . Thus by the later epochs of the Tertiary, the marine predator communities had begun to take on a modern aspect. Actual cases of predators in situ on prey, or of prey within stomach contents, provide compelling evidence for carnivory but are too rare to be of more than anecdotal interest. Notable examples include fossil asteroids (starfish) in situ on probable bivalve prey from the Devonian of New York and specimens of fish from various units, particularly the Cenozoic Green River Formation, with partially swallowed smaller fishes inside them (see p. 305) . Certain late Palaeozoic sharks similarly display stomach contents, including fragments of brachiopods and crinoids .

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A second source of data on ancient predation comes from the trace fossil record . Traces of successful or attempted predatory attacks include the distinctive marks made by biting and gnawing of predators on hard shells as well as drill holes of predatory molluscs (Fig. 1 ) . Bite marks provide strong indications of predatory attack, although they usually cannot be linked to specific predators. Ex­ ceptions include several instances of circular punc­ tures in Carboniferous ammonoids; the size and spacing of the holes implicates the associated cladodontid shark Symmorium as the predator. Classic examples of bite marks are known from Cretaceous ammonoids, where the holes match the size and spacing of the teeth of associated mosasaurs (Fig. lA) . Sublethal, healed fractures and punctures are common in certain types of Palaeozoic brachiopods and bivalves (Fig. 1C, D) . Alexander (1981, 1986) recognized lethal and sublethal (healed) shell dam­ age in assemblages of Ordovician to Pennsylvanian brachiopods, and observed an increased proportion

371

of lethal fractures in the later Palaeozoic. Together with the decline in frequency of repaired damage, this evidence suggests an increased intensity and effectiveness of predatory attack. Vermeij (1977) similarly documented trends in healed breakage amongst post-Palaeozoic molluscs, primarily gastro­ pods . Distinctive scalloped fractures in the outer lips of the gastropod shells can be identified as having been made by peeling crustaceans (Fig. lE) . The oldest instances of this lip-peeling type of frac­ ture are known from the Middle Ordovician, but case studies from the Ordovician and Silurian suggest that lip-peeling was exceedingly rare . In contrast, about 10-20% of individuals in some Devonian gastropod assemblages have suffered peeling, indi­ cating levels of predation comparable to those of the Late Palaeozoic (Schindel et al. 1982) and Mesozoic (Vermeij 1977, 1987) . Shell repair cannot be inter­ preted unambiguously because it monitors not only predatory attack, but also the ability of shells to resist attack . In contrast, the boreholes of carnivores testify to lethal attacks . However, it is critical to distinguish between non-predatory, domichnial borings and those produced by predators or parasites on live organisms . Carriker & Yochelson (1968) noted sev­ eral diagnostic characteristics of the latter, including penetration through a single valve, few holes per shell, holes drilled perpendicular to shell surfaces, and evidence for prey and site selectivity . The earliest evidence for drilling predation is derived from the Early Cambrian problematical, discoidal fossil Mobergella which displays minute drill holes in selective positions indicating probable predatory attack. Small cylindrical borings are also known through much of the Early Palaeozoic, although the affinities of these and the habits of their producers are not well understood. Many may have been produced by semiselective parasites living within the sediment. However, the first boreholes likely to have been made by gastropods occur in Devonian rocks . Circular- parabolic holes, closely resembling those produced by naticid gastropods, from the Middle Devonian of New York State, display a considerable degree of host and site selection (Fig. IF), as well as the presence of a raised boss in the centre of incomplete holes, which is often considered diagnostic of the naticid gastro­ pod mode of boring. Similar holes on related prey species are known from the Carboniferous . How­ ever, it appears that this early group of predaceous snails, probably a clade of archaeogastropods, be­ came extinct at the end of the Palaeozoic. The drilling

372

4 Palaeoecology

habit re-evolved during Middle - Late Triassic times, probably by a group of Mesogastropoda that became extinct before the end of the Triassic. Gastropod boreholes of both muricid and naticid affinity appear in the late Early Cretaceous (Albian) . Throughout later Cretaceous and Cenozoic times gastropod drilling became an extremely potent mode of predation in marine communities. Relatively high percentages of molluscs in some faunas dis­ play predatory attacks by gastropods. These snails show a great deal of stereotypy in their mode of attack and position of boring on the shells of prey (Reyment 1971 ) . Coprolites (Section 4 . 12) provide another trace of predation and their fossil record has been system­ atically documented by Hantzschel et al . (1968) . However, coprolites are very scattered and only a few specimens have been attributed directly to par­ ticular host species; notable examples occur amongst Jurassic ichthyosaurs, whose coprolites commonly contain fragments of molluscan shells . The third source of evidence for predation is a very indirect one, derived from apparent antipre­ dation adaptations in probable prey species . Signor & Brett (1984) noted a coincidence between the rapid diversification of durophagous predator groups and various trends in the skeletal mor­ phology of potential prey, starting in the Late Silurian to Devonian periods (Fig. 2) . Aspects of skeletal morphology that were adaptive for resist­ ance to predatory attack appeared rather abruptly in the Siluro-Devonian and increased toward the end of the Palaeozoic . Trends include the loss of umbilici in gastropods, and increased shell thickness and spinosity amongst brachiopods, gastropods, cephalopods, and crinoids (Fig. 2B) . Vermeij (1977) documented a great acceleration in the intensity of predation beginning in later Triassic and Jurassic times, which he termed the Mesozoic marine revolution . He noted the abrupt rise of durophagous groups such as crabs, stomatopods, and various shell crushing vertebrates, and docu­ mented several apparent antipredatory trends in molluscan groups . These include a tendency toward the evolution of thicker shells with narrow, toothed apertures, and the development of ribs and spines in several groups . Probable coevolution of predators and their prey may have promoted an increased diversity of defensive adaptations on the part of potential prey organisms . It would appear that the intensity of predation in marine systems has in­ creased rather steadily at least from Late Cretaceous times to the present day, and may be responsible in

part for the relatively higher species richnesses of many modern marine communities, as well as for many peculiar morphological adaptations of molluscan prey groups . References Alexander, R.R. 1981 . Predation scars preserved in Chesterian brachiopods: probable culprits and evolutionary conse­ quences for the articulates . Journal of Paleontology 55, 192- 203 . Alexander, R.R. 1986. Resistance to and repair of shell break­ age induced by predators on Late Ordovician brachio­ pods . Journal of Paleontology 60, 273 - 285. Bishop, G.A. 1975 . Traces of predation. In: R.W. Frey (ed .) The study of trace fossils, pp. 261 - 281 . Springer-Verlag, New York. Boyd, D.W. & Newell, N . D . 1972. Taphonomy and diagenesis of a Permian fossil assemblage from Wyoming. Journal of Paleontology 46, 1 - 14. Brett, c.E. & Cottrell, J . F . 1982 . Substrate specificity in the Devonian tabulate coral Pleurodictyum . Lethaia 15, 247-262 . Carriker, M.R. & Yochelson, E . 1968 . Recent gastropod bore­ holes and Ordovician cylindrical borings . Professional Paper of the United States Geological Survey No . 593B, B 1 - B23 . Hantzshel, W., EI-Baz, F. & Amstutz, G . c . 1968 . Coprolites: an annotated bibliography. Memoir of the Geological Society of America No. 108. Kauffman, E. G . & Kesling, R.V. 1960. An Upper Cretaceous ammonite bitten by a mosasaur. Contributions, Museum of Paleontology, University of Michigan 15, 193-248 . Massare, J.A. 1987. Tooth morphology and prey preference of Mesozoic marine reptiles . Journal of Vertebrate Paleontology 7, 121 - 137. Massare, J.A. 1988 . Swimming capabilities of Mesozoic marine reptiles : implications for mode of predation. Paleo­ biology 14, 187-205 . Reyment, R.A. 1971 . Principles of quantitative paleoecology. Elsevier Science Publishing, New York. Schindel, D . E . , Vermeij, G.J. & Zipser, E . 1982 . Frequencies of repaired fractures among Pennsylvanian gastropods of north-central Texas . Journal of Paleontology 56, 729 - 740 . Signor, P.W. & Brett, C . E . 1984. The mid-Palaeozoic precursor to the Mesozoic marine revolution. Paleobiology 10, 229 245 . Smith, S . , Thayer, C.W. & Brett, C . E . 1985 . Predation in the Paleozoic: gastropod-like drillholes in Devonian brachio­ pods . Science 230, 1033 - 1035 . Vermeij, G.J. 1977. The Mesozoic marine revolution: evidence from snails, predators, and grazers. Paleobiology 3, 245 258 . Vermeij, G.J. 1987. Evolution and escalation . Princeton Uni­ versity Press, Princeton, New Jersey .

4 . 1 3 Predation

4 . 1 3 . 2 Terrestrial J . A . MASSARE & c . E . BRETT

Arthropods

The first partially terrestrial animals, myriapods of Early Silurian (Llandoverian) age, apparently were predaceous and fed upon small aquatic animals (Niklas 1986) . Later Palaeozoic terrestrial arthropods (collembolans, insects, mites) were primarily her­ bivorous; however, in the Carboniferous certain large insects of the Order Protodonata, as well as spiders, specialized as predators on other insects . During the Mesozoic and Cenozoic a number of terrestrial arthropod groups (e.g. spiders, many beetles) became specialized as predators . Tetrapods

The first terrestrial vertebrates, early labyrinthodont tetrapods, were probably entirely predaceous, feed­ ing on fish and other aquatic animals, as well as smaller amphibians . These predators, beginning with the ichthyostegids in the Late Devonian, possessed sharp, spike-like, and undifferentiated teeth for impaling prey. Maximum usable prey size was limited by the size of the mouth gape . Later, the evolution of shearing-type teeth in the peleco­ saurs permitted active slicing, and thus consump­ tion of larger bodied prey animals . Herbivorous land vertebrates do not appear in the fossil record until the Late Carboniferous and carnivores con­ tinued to outnumber herbivores until at least the Middle Triassic . The shift toward increased numbers of herbivores is associated with the origin of therapsids in the Middle Permian . This transition may have been related, in turn, to the desiccation of coal swamps and concomitant loss of the palaeo­ dictyopteran insect fauna (Niklas 1986) . Bakker (1977, 1986) subdivided terrestrial tetrapod communities into four great groupings or mega­ dynasties, based on dominant herbivore and carni­ vore types; he stressed increasingly complex predator-prey interactions and, to a large extent, decreasing predator : prey ratios through time . Bakker used ratios of estimated biomass of predators to that of potential prey species, in particular, based on well preserved local fossil assemblages, to make inferences regarding metabolism and lifestyle of carnivorous tetrapods .

373

Megadynasty I. Early terrestrial ecosystems of Megadynasty I (Carboniferous -Early Permian) were dominated by primitive reptiles and amphi­ bians . The top predator was the synapsid reptile Dimetrodon, which was almost certainly ectothermic (cold-blooded), as evidenced by bone micro­ structure . Predator : prey ratios in these terrestrial ecosystems were characteristically high: large bio­ masses of predators were supported by small popu­ lations of moderate sized herbivores .

II. Megadynasty 11 (Early Permian ­ Middle Triassic) is referred to as the time of proto­ mammals, indicating dominance by the mammal-like therapsid reptiles (Fig. lA) . A variety of osteo­ logical and morphological evidence indicates that therapsids were endothermic (warm-blooded) (see Bakker 1977; Benton 1979) . Therapsids include di­ verse carnivorous, insectivorous, and herbivorous species . In populations from the Karoo beds of South Africa, predator : prey ratios average about seven per cent, only slightly higher than modern mammalian systems . The age of protomammals involved three waves of diversification (dynasties) and lasted approximately 15-20 Ma before giving way to Megadynasty III in Late Triassic times . The Middle Permian (Kazanian) witnessed an explosive adaptive radiation of predatory therapsids, the largest of which were bear-sized, dome-headed anteosaurs . These predators were substantially more diverse than those of the Early Permian, including five families, as opposed to the single Sphenacodontidae which had previously occupied the role of large predator. The Kazanian therapsid fauna was decimated by a mass extinction and replaced in Late Permian (Tartarian) time by newly evolved groups of therapsids dominated by predatory, sabre-toothed dicynodonts; low predator : prey ratios (5- 12%) prevailed . In turn, the Tartarian fauna underwent a mass extinction at the end of the Permian and elimination of all top predators enabled two new groups to expand into that role during Early Triassic (Scythian) time: the dog-like cynodont therapsids and, more signifi­ cantly, archosaurs belonging to the Erythrosuchidae (Fig. 1B) . The latter are forerunners of the thecodonts, including the crocodile-like phytosaurs and proterochampsids, which occupied roles of both top- and medium-to-small sized predators during the Middle - Late Triassic. Coevolution of prey defences is indicated by the appearance of heavily armoured aetosaurs . Bakker (1986) argued that the evolutionary re-

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374

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placement of therapsid predators by theocodonts is consistent with osteological evidence for endo­ thermy in these archosaurs . Conversely, Benton (1979) contended that the increasingly arid climates of the Triassic favoured archosaurs because they were ectothermic; he noted that ectotherms need to eat less and can conserve water better than endotherms .

III . Megadynasty III (Late Triassic ­ Cretaceous) was the age of dinosaurs . Bakker documented low predator : prey ratios within dinosaur dominated communities, suggesting high metabolic rates among theropod dinosaurs, resem­ bling those seen in modern predaceous mammals . This appears t o corroborate other osteological and

Megadynasty

physiological evidence which indicates that dino­ saurs were warm-blooded and active social creatures (but see Benton 1979) . Bakker (1986) documented a Mesozoic 'arms race' between dinosaurian predators and prey . Early predators included the Late Triassic coelurosaurs : slender, agile, and bipedal predators with teeth specialized for forming long slashing wounds. Later predatory carnosaurs displayed an enormous in­ crease in size from two-ton Allosaurus to five-ton Tyrannosaurus . Early theropods (e .g. Ceratosaurus) had a flexible lower jaw enabling them to gulp large chunks of flesh . Later, jaw flexibility was sacrificed in favour of a firm, strong bite . Even the large Tyrannosaurus had extremely well developed hind limbs and feet capable of sustained, relatively

4 . 1 3 Predation high running speeds. Other lineages of saurischian dinosaurs evolved different mechanisms for killing prey. A spectacular example is the Cretaceous species Deinonychus which possessed huge, curved, sabre-like claws for impaling and slashing prey . Baryonyx, from the Lower Cretaceous of the U.K. possessed extremely large claws on the front limbs, which it apparently used to hook prey much in the way that grizzly bears utilize their claws to catch salmon. In turn, Mesozoic herbivorous dinosaurs re­ sponded to the increasingly efficient and large predators by evolving a variety of defences . The sauropods took refuge in their large size . Bakker (1986) argued that they were also capable of some evasive action and perhaps could ward off attacks by swinging their large tails and battering their predators. Evidence from trackways suggests herding behaviour in brontosaurs which presum­ ably was a defensive social strategy in response to predation pressure on the young. Juvenile dinosaurs were maintained near the centres of migrating herds to be protected by adults, much in the fashion of herds of large ungulate mammals today. Other dinosaurs, particularly Ornithischia, evolved more spectacular defense strategies . Stegosaurs not only had large bony plates on the vertebral column, but also possessed a tail armed with sharp spikes which was clearly a formidable defensive weapon. Ankylosaurs evolved extremely rigid armour plating over much of the body, and in some cases (e . g . Ankylosaurus) possessed a huge bone-crushing club at the end of the tail . Perhaps the most spectacular of the defensive weaponry was that of the ceratopsian dinosaurs (e .g. Triceratops) . The massive heads of these Cretaceous dinosaurs were armoured with a heavy shield and adorned with one to five sharp horns, which could impale enemies . Dinosaurian predators of the Mesozoic were joined by a variety of other predatory vertebrates . From Triassic times onward, crocodiles were im­ portant predators in freshwater bodies . The early birds, from the Jurassic Archaeopteryx to the end of the Cretaceous, were entirely carnivorous and apparently evolved directly from small predatory coelurosaurids dinosaurs . In addition, pterosaurs occupied many predatory niches presently occupied by numerous birds.

Megadynasty IV. Although mammals, including insectivorous species, originated in the Triassic approximately contemporaneously with dinosaurs, and their diversity exceeded that of archosaurs by

375

the Late Cretaceous, mammalian predators re­ mained small with no large predatory species until the Early Palaeogene . The rise of the larger mammals of Megadynasty IV is a spectacular case of ecological replacement following on from the extinction of the dinosaurs . The earliest eutherian mammalian predators of the Tertiary, the arctocyonids, had five spreading clawed digits, short highly flexed limbs, and thick muscular tails. They were probably capable of climbing, digging, holding prey, and running over uneven or vegetated terrain. Generalized in loco­ motor and feeding adaptations, these forms gave rise to both the early carnivores and herbivores . The middle and late Palaeocene mesonychids im­ proved upon the primitive form with stiffer, more elongate limbs as adaptations for a more cursorial mode of life . The second wave of mammalian pred­ ators, the Creodonta, evolved advanced dental adaptations for meat eating - carnassial teeth . Hyaenodonts were the main cursorial predators and the stocky, more heavily built oxyaenids were the ambush predators . True carnivores (Order Carnivora), the third wave of mammalian predator diversification, appeared in the Late Eocene, and coexisted for a while with the creodonts (Bakker in Fatuyma & Slatkin 1983) . The earliest true carnivores were small weasel-sized viverids and myacids . The predator communities of the White River Badlands U . s . A . provide a glimpse of a Middle Tertiary com­ munity . Such Oligocene communities were a mix­ ture of archaic and modern carnivores . The predators were predominantly small-sized (less than 60 kg) . Locomotor adaptations suggest that there was an emphasis on climbing ability or short-distance ambush predation, but there were cursorial predators as well. The fauna lacked bone-crushing carnivores comparable to modern hyaenas (Stanley et al . in Fatuyma & Slatkin 1983) . In the Late Oligocene and Early Miocene, pred­ ator communities began to take on a more modern aspect. Dogs, some bear-dogs (amphicyonids), and, later in the Miocene, the hyaenas independently evolved the long-limbed, fleet-footed adaptations of running predators . From the Oligocene onward members of the cat family filled most of the ambush predator niches . The sabre-tooth cat lineage in­ cluded heavily built forms that specialized in prey­ ing on large, relatively slow-moving ungulates . Their demise was probably related t o the extinction of most of their large, herbivore prey species at the end of the Pleistocene . The second lineage of cat evolution, which survives today, included generally

376

4 Palaeoecology

smaller species that were built for greater agility. They specialized in faster, smaller prey . Thus the evolution of predators in the Northern Hemisphere was a series of radiations, each beginning with fairly unspecialized forms, often as primitive or more so than the pre-existing predator groups . Suc­ cessive radiations evolved better cursorial and den­ tal adaptations, climaxing in the predator faunas of the Late Pleistocene . The predator faunas of the island continents in the Tertiary were quite different. Giant birds occupied the cursorial predator niches in South America until the Pliocene, when the Central American land bridge allowed North American predators to invade South America. The South American ambush predators were cat-like mar­ supials that show striking parallels with the true cats of the northern hemisphere . In Australia, a variety of wolf-like marsupials filled the terrestrial cursorial predator niches . Study of Cenozoic and Recent mammalian pred­ ator guilds indicates that predator diversity is tightly correlated with prey richness (Van Valkenburgh 1988) . Furthermore, the basic array of predator feed­ ing types has remained relatively constant for at least 32 million years, despite great taxonomic turnover. Van Valkenburgh concluded than competition has played a key role in the maintenance of this diversity. Although mammals clearly dominated the large predator guilds during Cenozoic time, other ver­ tebrates have become highly successful in the roles

of smaller to medium sized predators. Lissamphibia (e . g . frogs, toads) have become specialized at insect capture . The rise of these amphibians, together with small rodents, has also triggered a major adaptive radiation of snakes, specializing in whole­ prey ingestion as a result of highly flexible jaw articu­ lations. The rise of passerine birds tracks the adaptive explosion of their insect prey; a number of raptorial predatory birds also appeared in the Cenozoic.

References Bakker, R.T. 1977. Tetrapod mass extinctions - a model of the regulation of speciation rates and immigration by cycles of topographic diversity. In : A. Hallam (ed . ) Patterns of evolution as illustrated by the fossil record, pp . 439 -468. Elsevier, New York. Bakker, R.T. 1986 . The Dinosaur Heresies . William Morrow Co. , New York. Benton, M.J. 1979 . Ecological succession among late Palaeo­ zoic and Mesozoic tetrapods. Palaeogeography, Palaeo­ climatology, Palaeoecology 26, 127- 150. Fatuyma, D . & Slatkin, M. (eds) 1983 . Coevolution . Sinauer Associates, Sunderland, Ma. Niklas, K.J. 1986. Large-scale changes in animal and plant terrestrial communities . In: D.M. Raup & D. Jablonski (eds) Patterns and processes in the history of life, pp. 383 405 . Dahlem Konferenzen, 1986 . Springer-Verlag, Berlin. Van Valkenburgh, B. 1988 . Trophic diversity in past and present guilds of large predatory mammals . Paleobiology 14, 155- 173.

4 . 14 Parasitism S . C O NWAY M O RRIS

Introduction

Parasitism is a symbiotic association whereby an individual derives nutritional benefit at the detri­ mental expense of another, by means of a long-term association. Usually such individuals concerned are separate species, but intra specific parasitism, such as that typified by the stunted male fused to the female ceratioid angler fish of the deep sea, is not unknown. Clearly, this definition of parasitism may grade into other types of symbiosis (e . g . commensalism), a s well a s the protracted predatory

activity that is typical of many bloodsuckers (e. g . ticks, lampreys) . In addition, the concept o f para­ sitism may be expanded to include species with a parasitic stage at some point in their life cycle, usually juvenile . These so-called parasitoids charac­ terize many phytophagous insects, and indeed if parasites and parasitoids are taken together they probably outnumber free-living species on the planet today. However, despite the abundance of parasitic species in all habitats, and the fact that there are representatives in the majority of metazoan phyla

377

4 . 1 4 Parasitism (conspicuous exceptions include the echinoderms, brachiopods, and other lophophorates), their fossil record is lamentable . This is because of the soft­ bodied nature of most parasites and their normal location in soft tissues with a minimal preservation potential (e . g . gut, muscle), combined with a general absence of effect on hard skeletal tissues . Further­ more, even when a pathological disturbance of hard parts can be assigned with confidence to parasitic inflammation, it is often impossible to identify the group responsible . However, although the evidence for fossil parasites is both slender and widely scat­ tered (Conway Morris 1981; Hengsbach 1990), in principle such a record could throw new light on host- parasite relationships . Major questions include : How did such associations arise? Was it by deterioration from a more benign symbiosis or does the parasitic condition arise abruptly from a free­ living form? To what extent do parasites coevolve with their hosts, or are their rates of evolution and cladogenesis more or less unrelated to that of the host? How do parasites weather host extinction, especially in cases of strict host-specificity?

The fossil record of parasites Several phyla are particularly important as parasites, but nearly all lack preservable hard parts and their body fossil record is scanty. Of the platyhelminthes, even the fossil record of the largely free-living turbellarians is highly questionable, while no fossils are known of the parasitic cestodes, trematodes, and monogeneans. Similarly, the sparse nemertean fossil record contains no obviously parasitic species. However, amongst the nematodes, a scattered record of free-living species (mostly from Cenozoic ambers) is augmented by a few parasitic forms . These include examples from Eocene lignites in East Germany, where beetles have been parasitized by nematodes (Fig. lA). In the Baltic ambers other nematodes occur in close association with a dipteran (Fig. 18), and an investigation of New World ambers may well reveal other parasitic associations that will supplement existing reports of free-living examples . Parasitic nematodes have also been reported from mammals entombed in the Siberian permafrost, but the most esoteric location is within a kidney stone of a cave bear from the Pleistocene of Germany . Saprobiotic nematodes described in association with a Carboniferous scorpion could be of relevance if such a life habit was a precursor to true parasitism . However, some nematologists refute the identifi­ cation of these fossils as nematodes, and if this is

c

D

A, The nematode Heydenius antiquus protruding from a cerambycid beetle Hesthesis immortua Oligocene lignite, East Germany. (After Heyden 1862 . ) B, Three nematodes (Heydenius matutinus) associated with a dipteran; Baltic amber, Oligocene. (After Menge 1866 .) C, Notopocorystes stokesi with swelling (lower right) on branchial region of cephalothorax, attributed to a bopyrid isopod; Albian, southern England. (After Forster 1969 .) D, Pithonoton marginatum with swelling (lower left) on branchial region of cephalothorax, attributed to a bopyrid isopod; Upper Oxfordian, Poland. (After Radwanski 1972.) Scale bars equivalent to 1 mm (A, B), 10 mm (C), and 5 mm (D) . Fig. 1

accepted their taxonomic placement becomes debat­ able . The nematomorphs, which are probably re­ lated to the nematodes, are free-living as adults, but a parasitic larva has been identified in association with fish remains in Eocene lignites from East Germany. No fossil acanthocephalans are known . However, on the basis of a proposed relationship with the free-living priapulid worms, putative ancestral types were identified amongst the prolific priapulid fauna in the Middle Cambrian Burgess Shale (Conway Morris & Crompton 1982) . More recently, however, an alternative relationship - between acanthocephalans and rotifers has been advanced . The arguments rely largely on ultrastruc­ tural comparisons and some proposed organ homo­ logies, but the fossil record is unlikely to assist in this matter as fossil rotifers are not known. If the record of parasitic fossil worms is slender, that of parasitic arthropods is only marginally more satisfactory. Parasitic insects are best known from the Cenozoic, with ambers yielding some of the

378

4 Palaeoecology

finest examples. Mesozoic examples are more limi­ ted, but include Cretaceous ?fleas, whose presence has been used to infer the nature of the original hosts . Arthropod - plant relationships have been traced back to the early stages of terrestrial invasion in the Oevonian, but accepted examples of parasitic activity in the form of plant galls do not appear until substantially later. Although the earliest putative examples are Permian, the bulk of the record is from the Cainozoic. In the marine realm a moderately secure record is available from the Jurassic onwards . The most striking examples are siphonostome copepods that were recovered from gill chambers of Lower Cretaceous fish; their exceptional preservation is a result of diagenetic phosphatization . The activity of parasitic copepods has been inferred also from galls on echinoderms that range in age from Jurassic to Miocene . Evidence for the activities of other para­ sitic arthropods in marine communities is entirely dependent on what are effectively trace fossils. The most impressive roster of examples comes from the swellings in the branchial regions of decapods (Fig. 1 C, 0); these are attributed to the activity of parasitic isopods (Epicaridea) . Although it has been tra­ ditional to ascribe these manifestations to members of Bopyridae, the absence of the actual isopods in the branchial chambers make such assignments somewhat tentative . The first examples of infes­ tation are recorded from the Upper Jurassic but, despite a rise in the number of species parasitized towards the end of the Jurassic, thereafter such examples appear to be rare in the fossil record. Whether decapods were able to evolve resistance to infestation over geological time is not known. Finally, amongst the isopods, a possibly parasitic species has been described from the Cretaceous of Texas. Although most cirripedes (barnacles) are free­ living, the parasitic ascothoracicans are represented by characteristic borings and cysts in Cretaceous echinoids and octocorals. However, the cancer-like rhizocephalan cirripedes, the adult of which forms a ramifying mass in the host tissue, appear to have been unrecognized in the fossil record . Excluding leeches, which have a questionable fossil record from the Silurian and Jurassic, the record of parasitic annelids is effectively confined to the myzostomids . In Recent faunas these unusual organisms infest echinoderms, especially crinoids, and may provoke cyst-like swellings . It is, therefore, not surprising that many of the galls and other swellings in fossil echinoderms have been attri-

buted to myzostomids, but the great majority of such identifications are suspect. Reasonably secure examples, however, are known from the Middle Palaeozoic onwards, but the number of convincing examples is low (Arendt 1985) . Another popular culprit for other excavations in echinoderms (especially those that are cup-shaped) are parasitic gastropods . Analogues in the Recent suggest that some (especially from Cretaceous echinoids; Kier 1981) are probably correctly assigned . However, considerable doubt surrounds many others from Palaeozoic and Mesozoic echino­ derms, especially as the coelomic cavity usually appears to have remained untapped by the putative gastropod . These galls, excavations, and other dis­ turbances are widespread in fossil echinoderms (Fig. 2A, C, 0, F), being well preserved because of the ability of stereom tissue to mould itself to local disturbances . However, thE nature of the irritant is usually problematical, and in many cases it is ques­ tionable whether they can be usefully classified as parasitic interactions . This is because in many instances sections of the disturbed area give no clues as to the nature of the possible organism that provoked the reaction . A notable exception is pro­ vided by the funnel-shaped phosphatic structures referred to Phosphannulus (Fig. 2E) . These have been found within perforated swellings on crinoid stems, ranging from Ordovician to Permian . Although the affinities of this organism are speculative, it appears that having settled on the surface of the crinoid stem it enveloped itself within the stereom, main­ taining a connection with the exterior and also establishing a link to the central canal, from which it may have derived nourishment. What appear to have been free-living examples of Phosphannulus, however, are also known, including the earliest examples from the Upper Cambrian . It seems pos­ sible, therefore, that the genus was a facultative parasite, although particular species may have been wedded to a particular mode of life . The catalogue of other possible parasitic inter­ actions is lengthy, but relatively inconclusive . Some pathologically deformed fossils, including ammon­ ites (Morton 1983), may reflect parasitic infestation . More specifically, the formation of a pearl in modern bivalves is frequently provoked by the settling of a parasitic larva, often that of a trematode, and its subsequent encapsulation by the irritated mantle tissue . The fossil record of pearls is slender, but in bivalves extends back to examples in the Silurian of Bohemia (Kriz 1979) . Whether these examples (and possibly similar structures noted in Oevonian

4 . 14 Parasitism

379

Fig. 2 A, Swelling and associated pits on crinoid stem; Silurian, Gotland . (After Franzen 1974.) B, 'Tubotheca' from the graptolite Dictyonema; Ordovician, Sweden . (Photograph courtesy of P.R. Crowther . ) C, Gall-like swelling with two pits on calyx of the crinoid Eucalyptocrinites caelatus; Silurian, Ontario. (From Brett 1978 . ) D, Gall-like swellings on a crinoid stem; Devonian, Morocco . (From Franzen 1974.) E, Transverse section of Phosphannulus in a crinoid stem (note axial canal at base of figure); Permian, Kansas . (From Welch 1976 . ) F, Inflated crinoid with central hole; locality uncertain. (From Franzen 1974.)

goniatites and Silurian tentaculites) can be at­ tributed to platyhelminth infestation is speculative, especially as its appears that a variety of foreign bodies could provoke pearl formation. Phosphatic calculi that occur in some residues with conodonts have been tentatively ascribed as a response to parasitic attack, while similar structures have been recorded also in association with Silurian bryozoans (Oakley 1966) .

Another category of disturbance that has been moderately well documented is a variety of galls and other tumour-like swellings in trilobites rang­ ing in age from Middle Cambrian to apparently the Devonian. The parasite is believed to have been housed beneath the exoskeleton and survived the moulting intervals of the host. However, its original nature is entirely speculative, and the lack of specific siting suggests that it may not have targeted a

380

4 Palaeoecology

particular organ. Other blister-like structures have been described from Silurian brachiopods (so-called Ziegler's blisters) and also graptolites, although whether the former are of parasitic origin is not certain. A more dramatic example of infestation in sessile members (dendroids and tuboids) of the latter group, however, is recorded by vermiform tubules (Fig. 2B) that extend from the colony. These 'tubothecae' consist of immensely thickened cortex, and evidently represent an attempt by the zooids of the colony to encapsulate the parasite by secretory organs that in normal circumstances were employed in constructing the periderm. That these attempts were unsuccessful is evident from the open distal aperture of the tubotheca. Although the cortical coating appears to have mimicked the vermiform nature of the parasite, its affinities are unknown and so far as is known the related pterobranchs of the Recent do not host similar parasites . Examples of vermiform traces within rugose corals have been ascribed to parasites that gained access to the gastric cavity in order to gain food (Oliver 1983) . Although numerous Recent protozoans are known as parasites, the lack of hard parts and minute size means that the fossil record is effectively non-existent. Possible examples of parasitic fora­ minifera are known from the Cretaceous, but this inference remains speculative . In addition, possible ectoparasitism by ciliates or amoebae on Ordovician chitinozoans was documented by Grahn (1981) . It can be seen, therefore, that although parasitic activity can be traced to the Cambrian, the record is invariably slender and presents more a series of isolated vignettes than a complete story. Documen­ tation is further hindered by the difficulty in de­ ciding whether some fossil symbioses are genuinely parasitic. In particular, a number of epizoans, in­ cluding those located within the mantle cavity of brachiopods and bivalves, probably verged on being parasites. It is noticeable, moreover, that un­ equivocal assignment of parasites to known groups is very seldom possible before the Jurassic, and it is no coincidence that the rise of modern faunas from this time strengthens uniformitarian assumptions . Future research

While the fossil record provides at present only the outline of the history of parasitism, there is hope that future investigations will extend present know­ ledge . The growing roster of exceptionally preserved biotas may lead to new discoveries, especially as nearly all parasites are either soft-bodied or have

only delicate skeletons. In some such Lagerstatten the quality of preservation of soft tissue, including muscles, suggests that encapsulated parasites may be identified. Another possibly fruitful source of investigation are coprolites, not least because many parasites release prodigious quantities of eggs whose tough walls would raise fossilization potential. Other symbiotic associations in the fossil record may provide useful analogies to the origins and evolution of parasitism. At present, e . g . , it is not clear whether parasitism arises from a shift of a more benign association, or represents a more abrupt invasion. It is, however, apparent that in some examples commensalism can persist for millions of years without the balance deteriorating to the detriment of one partner. One of the best known of such associations, that between Palaeozoic crinoids and their coprophagous gastropods (platy­ ceratids), persisted for c. 200 million years with­ out a shift towards a parasitic mode of life. There is also evidence that in some commensal associations the rate of morphological evolution in the host exceeds that of its partner. If the fossil record of a parasitic association could be traced in sufficient detail, it might be possible to determine whether the parasite weathered host extinction. Particular interest revolves around monospecific associations, as the adaptive advan­ tages of having a restricted host repertoire are not always apparent. It may be that an escape avenue is opened by paedomorphic mutants restricting their life style to the secondary host, until a new primary host can be found after the extinction event. Such evolutionary 'bottle-necks' may well be of particular importance in driving parasite evolution.

References Arendt, Y.A. 1985 . Biotic relationship of crinoids . Paleonto­ logical Journal 19, 67- 73. Brett, C.E. 1978 . Host-specific pit-forming epizoans on Silurian crinoids . Lethaia 11, 217-232 . Conway Morris, S. 1981 . Parasites and the fossil record . Parasitology 82, 489-509 . Conway Morris, S . & Crompton, D . W . T . 1982 . The origins and evolution of the Acanthocephala. Biological Reviews 57, 85 - 1 1 5 . F6rster, R. 1969 . Ep6kie, EntOkie, Parasitismus und Regener­ ation bei fossilen Dekapoden. Mitteilungen der Bayerischen Staatssammlung for Paliiontologie und historische Geologie 9, 45 -59. Franzen, C . 1974. Epizoans on Silurian- Devonian crinoids . Lethaia 7, 287-301 .

4 . 15 Palaeopathology Grahn, Y. 1981 . Parasitism on Ordovician Chitinozoa. Lethaia 14, 135- 142. Hengsbach, R. 1990. Die Palaoparasitologie, eine Arbeit­ srichtung der PaHiobiologie . Senckenbergiana Lethaea 70, 439 -461 . Heyden, C . 1862 . Gliederthiere aus der Braunkohle des Niederrhein's der Wetteran und der Rohn. Palaeonto­ graphica 10, 62- 82. Kier, P.M. 1981 . A bored Cretaceous echinoid . Journal of Paleontology 55, 656- 659. Kriz, J . 1979. Silurian Cardiolidae (Bivalvia) . Sbornik geologi­ ckych ved paleontologie Ustredni ustav geologicky, Praha 22, 1 - 157. Menge, A. 1866. Ueber ein Rhipidopteron und einige andere im Bernstein eingeschlossene Thiere. Schriften der Natur-

381

forschenden Gesellschaft in Danzig 3 (Ser. 8), 12 - 15 . Morton, N . 1983 . Pathologically deformed Graphoceras (Ammonitina) from the Jurassic of Skye, Scotland . Palae­ ontology 26, 443- 453. Oakley, K.P. 1966 . Some pearl-bearing Ceramoporidae (Polyzoa) . Bulletin of the British Museum (Natural History), Geology Series 14, 1 -20 . Oliver, W.A. 1983. Symbioses of Devonian rugose corals . Memoir of the Association of Australasian Palaeontologists 1, 261 -274. Radwanski, A. 1972. Isopod-infected prosoponids from Upper Jurassic, Poland. Acta Geologica Polonica 22, 499 506 . Welch, J.R. 1976 . Phosphannulus on Paleozoic crinoid stems. Journal of Paleontology 50, 221 .

4 . 15 Palaeopathology L . B . HALSTEAD

Introduction

Palaeopathology is the study of ancient disease and, by its very nature, must be restricted to lesions that affect fossilizable materials . The healing of shells damaged during life is commonly observed, but only among vertebrates, with their internal skel­ etons, have any systematic attempts been made to study trauma and disease . Palaeontologists have often failed to recognize the effects of disease, and hence misinterpreted material. This is exemplified by the description of the first complete skeleton of Neanderthal man . For most of the twentieth century, reconstructions of Neanderthal man have portrayed a shambling, almost ape-like posture with a bull-neck and head thrust forward - the stereotype of our brutish caveman ancestor. Apart from the incisors this individual had lost all his teeth and must have been about 60 years old. The neck vertebrae were severely distorted by osteoarthritis, as indeed was most of the vertebral column. The posture and gait attributed to this skeleton may have been accurate, but they were of a diseased old man and were not attributable to the rest of his race . The problems of interpreting fossils may be com­ pounded when medical scientists identify features resulting from the processes of fossilization as pathological conditions. For example, it was claimed that a small coelurosaur dinosaur Compsognathus died from tetanus because the posture in death

mirrored that of a tetanic spasm. In fact, a drawing back of the head and raising of the tail in articulated skeletons is a normal consequence of flesh rotting away and shrinkage of fibrous connective tissue of ligaments, so the posture is entirely a post-mortem effect. Some lesions are quite unambiguous, such as the wound in the skull of an Oligocene false sabre­ tooth cat Nimravus which was stabbed in the head by a sabre-tooth Eusmilus. Although there was severe damage to the frontal sinuses, the wound healed . Nothing could have inflicted such a wound apart from the canine of a sabre tooth . In some instances, simply the pattern of tooth marks enables the nature of the predator to be identified; it may even be possible to reconstruct an attack in fine detail, as in the case of one ammonite bitten 1 6 times by a (presumably inexperienced) mosasaur. Fracture healing

The vertebrate skeleton (especially the limb bones) may fracture when subjected to sudden trauma. However, bone has the ability to regenerate dead and broken parts, and healed fractures are not un­ common among fossil vertebrates . Generally, limb bone fractures occur in young animals, although they carry evidence of such events throughout their lives . Fracturing of limbs in adult animals usually leads to death and, as there is no sign of healing, it is not possible to determine whether the break

382

4 Palaeoecology

occurred during the animal's life or is a post-mortem effect . The normal processes of fracture healing can pro­ duce bony structures that are easy to misinterpret. The first stage in fracture healing is the formation of a blood clot or haematoma callus, together with the necrosis or death of bone adjacent to the fracture . The haematoma is replaced by fibrocartilage but, on occasion, may become ossified . The original femur of Java Man, Pithecanthropus erectus (now known as Homo erectus), has an extensive, irregular bony ex­ crescence on the upper part of the shaft; this has been interpreted as a bone cancer but probably represents the ossification of a haematoma . The next stage in healing is the growth of a bony callus that completely surrounds and encloses the region of the fracture . Bony trabeculae replace the fibrocartilage callus, new bone is produced to re­ construct the limb bone and the necrotic bone is resorbed . Occasionally the bony callus is not resorbed, as occurred in a specimen of the sauropod dinosaur Apatosaurus where two tail vertebrae are united by a bony callus . This too has been inter­ preted as a bone cancer . There is a tendency for any evidence of the proliferation of bone to be attributed to cancer, whereas unequivocal bone cancer is vir­ tually unknown in the fossil record . Skeletal degeneration

Two major degenerative diseases affect the ver­ tebrate skeleton : osteoporosis and osteoarthritis . In osteoporosis, the compact cortical bone is thinned and the trabeculae of the cancellous bone are similarly reduced . The outward shape of the bone is un­ changed, but up to 75% of bone mass may be lost. No study of osteoporosis in the fossil record has been undertaken . Osteoporosis has been claimed among such marine reptiles as ichthyosaurs and plesiosaurs, but these are characterized by their light spongy bone - a feature of all aquatic tetra­ pods that is unrelated to this degenerative disease . Osteoarthritis is a disease of the joints associated with ageing; it seems to begin with an alteration of the nature of the synovial lubricating fluid oc­ casioned by disruption of the blood supply . The presence of blood in the fluid results in the lubricant ceasing to function adequately, so that the articular cartilage is plucked off. Eventually bone grinds directly onto bone, producing a highly burnished surface that looks like ivory and is termed eburnation . Abrasion of the bone induces a reactive proliferation around the margins of the joints . This

'lip ping' or osteophytosis can generally be taken as evidence of advanced osteoarthritis . On occasions, this reactive proliferation may result in the fusing or ankylosis of adjacent bones. The fusion of dino­ saur vertebrae in the mid dorsal region has been attributed to osteoarthritis but, as it only ever affects the two mid dorsal vertebrae, this particular fusion cannot be pathological . A case of initially unrecognized osteoarthritis was present in a Jurassic shortnecked plesiosaur, Lio­ pleurodon macromerus, where progressive in­ crease in lipping of the vertebral centra of the neck was carefully documented in the description of the skeleton; in fact, this was a typical example of osteophytosis (Tarlo 1959) . Common examples of osteoarthritis were found among fossil cave bears . During their hibernation, the greatest mortality occurred among (1) young bears who had been unable to accumulate enough fat to see them through the winter; and (2) slow, old bears, who similarly had been unable to obtain sufficient food . The old bears were generally suf­ fering from osteoarthritis, as evidenced by the osteophytosis of their vertebrae (Fig . 1). Infections o f the skeleton

Evidence for bacterial infections comes from their indirect effect on the skeleton . When infection in-

Fig. 1 Arthritic vertebra from Pleistocene cave bear . (From Halstead & Middleton 1972 . )

4 . 1 5 Palaeopathology vades the skin so that it reaches the surface of the bone, the periosteum is infected (a condition termed periostitis) and this in turn affects the underlying bone . The surface becomes necrotic and develops a characteristic pitted texture . If the infection invades the cavity of the bone, the condition is termed osteomyelitis . Bacteria proliferate and pus accumu­ lates within the cavity. Sinuses develop to drain away the pus and large areas of bone become necrotic. The necrotic bone is replaced by bony outgrowths developed from the surviving healthy bone . This mixture of necrotic and proliferating tissue gives the bone a characteristically roughened surface (Fig. 2) . Where bacteria gain entry into deep tissues, they may become 'walled up' to form an abscess . If this occurs adjacent to hard tissue (such as alongside the root of a tooth) a cavity is eroded to accommodate the developing abscess . This can be seen in the teeth of large mammals, such as elephants (Fig . 3; Bricknell 1987) . A more direct involvement in the destruction of skeletal tissues by bacterial infection is seen in periodontal disease. At the edge of the gums, between the teeth, particles of comminuted food may become trapped . The bacteria create their own micro­ environment with a low pH, causing the tooth to be dissolved away at the gingival margin . This leaves a characteristic horizontal groove (Bricknell 1987), encouraging further infection, and facilitating the trapping of further food particles . Infection gradu­ ally travels down the periodontal membrane, the zone of collagenous fibres which embed the tooth in its alveolus or socket. Dental abscesses in par­ ticular develop at the apex of the roots of the teeth, where the travelling infection comes to rest. It is here that the cavitation of the roots and surrounding bone begins to develop . Patterns of disease

The study of skeletal diseases has concentrated on fossil man and, more recently, on animal remains from archaeological sites (Baker & Brothwell 1980) . The palaeontological literature has passing records scattered among the descriptions of fossils . Recently, in a preliminary study of diseases in Quaternary elephants, Bricknell (1987) documented the preva­ lence of certain diseases through time (Fig. 4) . The incidence of periodontal disease in particular showed a striking correlation with climatic changes . This may not have been a direct effect, and was more likely related to the greater diversity of plant

383

Fig . 2 Osteomyelitis of rib from woolly mammoth . (From Bricknell 1987 . )

Fig . 3

Cavity i n root o f tooth from straight-tusked elephant . (From Bricknell 1987.)

life and an increase in fruiting plants which pro­ vide a suitable substrate for the bacteria that cause periodontal disease . The distribution of other types of disease, such as other bacterial infections, follows a comparable pattern, but the Wolstonian cold period seems to have an unusually high incidence . Curiously, fractures of limb bones seem to be con­ fined to the interglacials, with the exception of the last (Devensian) glaciation . The distribution of osteoarthritis also seems to follow a climatic pattern, with an increased incidence in the warmer interglacials . There has always been an underlying assumption that, with the possible exception of diseases associ­ ated with ageing (such as osteoarthritis), prehistoric life was especially healthy . The results of Bricknell's survey suggest that patterns of disease match cli­ matic regimes . The spread of disease is often tacitly attributed to the activities of man, but this study of Quaternary mammals demonstrates the success of pathogenic bacteria in the more humid, warmer climatic regimes, without any encouragement from the activities of human beings .

4 Palaeoecology

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Pseudopathology

The study of palaeopathology requires a detailed knowledge of both pathology and the processes of fossilization . One of the major problems is in iden­ tifying specific pathologies and distinguishing them from pseudopathologies . The action of boring bi­ valves can simulate dental abscesses; burial in an acidic environment can result in the surface erosion of bone, which can mimic periostitis or even osteo­ myelitis . Even the excavation of fossil bones can produce pseudopathologies : depressed fracturing

Fig. 4 Distribution through time of disease and trauma in Quaternary elephants . (From Bricknell 1987.)

of skull bones may result simply from pressure on the overlying sediments, while digging implements can produce pseudohunting injuries . Erosion of the bone surface can often be produced by rootlets . Saprophytic fungi attack bone, and they are known from the time of the first bone preserved in the fossil record . In general, however, a close exami­ nation of the details of surface structure and also in cross-section (as a thin section under the light microscope) will determine the authenticity or otherwise of the supposed pathologies .

385

4 . 1 6 Trophic Structure References Baker, J . & Brothwell, D. 1980 . Animal diseases in archaeology. Academic Press, London and New York. Bricknell, I. 1987. Palaeopathology of Pleistocene proboscid­ eans in Britain. Modern Geology 11, 295 -309 . Brothwell, D. & Sanderson, J.T. 1964. Diseases in antiquity. Thomas Publications, London . Halstead, L . B . 1974. Vertebrate hard tissues . Wykeham Publications, London .

Halstead, L.B. & Middleton, J. 1972. Bare bones: an exploration in art and science. Oliver & Boyd, Edinburgh. Moodie, R. 1917. General considerations of the evidence for pathological conditions found among fossil animals. Science 4 3 , 425 -452. Tarlo, L . B . 1959 . Stretosaurus gen . nov . , a giant pliosaur from the Kimeridge Clay . Palaeontology 2, 39 -55. Wells, C . 1964. Bones, bodies and disease. Thames & Hudson, London.

4 . 16 Trophic Structure J . A . CRAME

One o f the most exciting breakthroughs in com­ munity palaeoecology in recent years was the dis­ covery that fossil assemblages can be classified according to the feeding characteristics of their con­ stituent species . This resulted in an entirely new way of comparing and contrasting palaeocommuni­ ties . The trophic structure of a community can be defined as the cumulative feeding habits of its com­ ponent species . These feeding habits are in turn based on two fundamentally different food chains: a grazing one centred on green plants and a detritus one centred on dead organic matter. Both these chains are terminated by predators . It is important to emphasize at the outset the distinction between feeding habit and trophic level. Whereas the former relates to what an organism eats, the latter refers to its position in the steps of energy transfer (Scott 1976) . Each species occupies a specific position (or positions) in a food web (Fig. 1 ) . Marine biologists had, o f course, been classifying feeding mechanisms for many years . However, their schemes were based largely on features such as food particle size, and little attention was paid to precisely what was eaten or where . These were just the sorts of details that were of interest to the community palaeoecologist, and, when added to existing schemes, produced a number of basic feed­ ing groups (or trophic categories) . Several simplified classification schemes for benthic marine inver­ tebrates are now in existence (Table 1) (Walker & Bambach 1974) .

When fossil communities were analysed using these new schemes, it became apparent that the vast majority of species fell into just three basic categories : suspension feeders, detritus feeders, and predators (Table 2) . In fact, so striking was this regular tripartite division that it was suggested that these categories could form the end members of a triangular (or ternary) diagram and be the basis of a rapid system for classifying palaeocommunities Table 1 A simplified classification of marine invertebrate trophic groups . (Adapted from data given by Walker & Bambach 1974.)

Group

Feeding habits

1

Suspension feeders

Higher level (epifaunal or infaunal)

2

Suspension feeders

Lower level (epifaunal or infaunal)

3

Deposit feeders

Sediment-water interface (epifaunal)

4

Deposit feeders

Shallow, in-sediment (infaunal)

5

Deposit feeders

Deep, in-sediment (infaunal)

6

Browsers

(Epifaunal)

7

Predators

(Passive or active; epifaunal or infaunal)

8

Scavengers

(Epifaunal or infaunal)

9

Parasites

386

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4 Palaeoecology

P R E DATO R S

CONSUMfRS s " ,pe",o feed ers

F i l te r feed ers

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1

PRO D U C E RS Table 2

RECUP ERA TORS Det r i t u s fe ed e rs Depos i t feed ers

B ro w s e r s

Scave ngers

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DET R I T U S

The relationship between feeding habit and trophic level . Within each of the basic food chains ( a consumer one based on green plants and a recuperator one based on dead organic matter), species of various feeding habits can be arranged into trophic levels at each stage of energy transfer. Heavy arrows energy-flow pathways; light arrows donors of organic detritus . (From Scott 1976.) Fig. 1

=

=

The principal marine invertebrate trophic groups (Data from Walker & Bambach 1974, and Scott 1976 . )

Group

Examples

Food and feeding method

1

Suspension feeders

Food - small particles such as phytoplankton and zooplankton; dissolved and colloidal organic molecules; resuspended organic detritus. Feed b y - flagellae, ciliated lophophores, ctenidia and tentacles .

Sponges, anthozoans, hydrozoans, stromatoporoids, bryozoans, brachiopods, many bivalves, some gastropods, some annelids and crustaceans, pelmatozoans and graptoloids .

2

Deposit feeders*

Swallow or scrape particulate organic detritus, living and dead smaller members of benthic flora and fauna, and organic-rich grains.

Some crustaceans, echinoids, ophiuroids, bivalves, gastropods and annelids; scaphopods, holothurians .

3

Predators

Either active search and seizure (involving swallowing whole, biting and chewing or external digestion) or passive (waiting for prey to pass) techniques.

Larger anthozoans, cephalopods, many gastropods, some annelids and crustaceans, asteroids, some echinoids and ophiuroids.

* In palaeontological studies, deposit feeders are usually included in the more general category of 'detritus feeders' . This also includes scavengers, which eat larger particles and dead organisms upon and within the sediment (e . g . some gastropods), and most browsers (or herbivores) . The latter are first level consumers that scrape, rasp, or chew live algae and other plants ( e . g . Amphineura and some gastropods) .

(Fig . 2; Scott 1976, 1978) . In practice, it was found that precise habitat requirements needed to be recorded too, and so a second 'substrate-niche' tri­ angle is usually depicted alongside the 'feeding­ habit' one (Fig . 2) . Substrate-niche names are usually appended as prefixes to the feeding-habit ones, giving a community a title such as 'vagrant­ epifaunal, detritus-suspension feeding' . One of the obvious applications of this method of describing trophic structure is in differentiating contemporaneous communities within particular environmental settings . For example, both Cretaceous and Cenozoic communities occurring along onshore - offshore gradients plot in distinctive fields within the ternary diagrams (Fig. 3; Scott 1978) . Although the database is still comparatively small, it is also possible to trace the trophic groups associated with certain habitats through time .

For example, in lower shore face and nearshore communities between the Early Palaeozoic and the Cretaceous, there was a marked shift from epifaunally- to infaunally-dominated detritus­ suspension feeding types (Scott 1976) . There are, of course, other ways of depicting the trophic structure of palaeocommunities . In his very detailed analysis of macrobenthic assemblages from the Korytnica Clays (Middle Miocene, central Poland), Hoffman (1977) used a series of tables to illustrate 'trophic- substrate - mobility niches' . These are simple two-dimensional diagrams which plot food location (infauna and epifauna, subdivided into mobile and sessile) against feeding category (suspension and deposit feeders, predators etc . , subdivided into various positions i n the water column and sediment) . Each of these diagrams is supported by a histogram showing the distribution

4 . 1 6 Trophic Structure

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4 Palaeoecology

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a

Trophic structure of three communities from the Middle Miocene Korytnica Clays, central Poland . Their frequent association is thought to reflect an ecological succession in a small shallow basin from a pioneer stage on barren muddy bottoms (Corbula community), through an intermediate stage (Corbula- scaphopod community), to a mature (climax) stage marked by the development of extensive seagrass stands (Turboella - Loripes community) . An index of trophic uniformity within each community is derived from the dispersion of total biovolume amongst the various trophic groups (upper histograms) . The index (or Nesis) value (6 2) is the total biovolume of the assemblage divided by the number of trophic groups (see Hoffman 1977, p. 244). The high value in the Corbula community (A) is due to the dominance by a single species (the shallow-burrowing, suspension­ feeding bivalve Corbula gibba) . Much lower values in the Corbula - scaphopod (8) and Turboella - Loripes communities (C) can be linked to the wider dispersion of biovolume amongst the various trophic troups . The trophic web reconstruction for the Corbula community (a) is a very simple one based largely on a short suspension-feeder food chain . However, in the succeeding Corbula - scaphopod community (b) the web is appreciably more complex, and comprises two distinct subwebs (the suspension-feeding and deposit-feeding ones) . Finally, in the climax Turboella - Loripes community (c) there are at least three equally important subwebs. Note that separate subwebs can be terminated by the same predator (top row of boxes) . epr epifaunal predators, ipr infaunal predators, sc scavengers, par parasites, br browsers, df deposit feeders, sf suspension feeders . (From Hoffman 1977, 1979.) Fig. 4

=

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of biovolumes (representing biomass) amongst the various trophic categories (Fig. 4) . In fact, the pres­ ervation of these assemblages was so good that trophic webs could be constructed for each com­ munity . Although this entailed estimating unpre­ served components of the ecosystem, and involved a considerable amount of simplification, the resulting models proved to be valuable aids in the study of community structure and function (Fig. 4) .

One potentially serious drawback to the tech­ niques outlined so far is the fidelity of the fossil record (Section 3 . 12) . Estimates of the proportion of a biocoenosis unlikely to be preserved (i. e . the soft­ bodied component) range from 50 to 75% . Deposit­ feeding groups of annelids and athropods are particularly likely to be missing from a fossil as­ semblage . There may, however, be ways of partially offsetting this problem. Firstly, there may be direct

389

4 . 1 6 Trophic Structure evidence of deposit feeders in the form of either faecal pellets or bioturbation . It may also be possible to calculate the proportion of individuals at various trophic levels in an assemblage and compare these ratios with those in a modern community. Using estimates of the efficiency of energy transfer be­ tween trophic levels of 10-20%, it may be clear, for example, that the ratio of carnivores to primary consumers is too high . In that case, soft-bodied organisms must have been an important component of the ecosystem (Stanton et al . 1981) . A trophic web based solely on numerical abun­ dances arguably gives a poor picture of the original community. Ideally, trophic analyses should be based on estimates of energy flow from one level to another and this would appear to�be beyond the scope of the palaeontologist. Nevertheless, in a pioneering study of molluscan assemblages from the Middle Eocene Stone City Formation of south­ east Texas, Stanton et al. (1981) suggested several ways in which abundance data could be refined to make them more representative of the passage of energy through a community . Such techniques, which are particularly amenable to certain predatory gastropod taxa, include the production of survivor­ ship curves (Fig. 5) . From these it is apparent that Polinices aratus, the numerically dominant predator, was subject to very high juvenile mortality . In at least five other predatory taxa (such as the fascio­ lariid Latirus moorei; Fig. 5), it was found that a much greater proportion of their populations at­ tained adulthood; these were thus inferred to have been more important components of the Stone City Formation foodweb (Stanton et al . 1981, Table 2) . Another useful measure of a species' significance in a trophic web may be its total biomass, for in predators this should be related to the biomass of prey consumed. The number of prey required to support a predator population is proportional to the amount of energy input necessary to produce and maintain the predator population (Stanton et al. 1981; see their Table 2 where biovolumes are used to calculate the biomass formed by secondary pro­ duction) . In the Stone City Formation, biomass values again showed that predatory gastropods, such as Latirus moorei, two species of turrids, and Retusa kellogii (opisthobranch), were much more prominent than Polinices aratus (the naticid) . The influence of the turrids is particularly important as they fed on non-preservable prey (primarily polychaetes) . If further turrids have similar size ­ frequency distributions, it has been estimated that the proportion of soft-bodied prey in the food web

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may have been as high as 50% . A more serious problem faced by the community palaeoecologist is that many benthic organisms defy simple trophic classification. Take, for example, those types that can readily interchange between deposit- and suspension-feeding strategies . These include representatives of several polychaete famil­ ies, a number of ophiuroids and irregular echinoids, and a significant proportion of the bivalve super­ family Tellinacea (species of Scrobicularia, Macoma, Tellina, etc. ) . By switching between these two feeding modes, organisms may well be able to over­ come periods of food shortage . This in turn would permit colonization of unpredictable habitats, such as estuaries or shallow temperate seas . Some recent discoveries from the deep seas have had a profound effect on our understanding of trophic structure . Not the least of these is the start­ ling revelation that many abyssal bivalves (perhaps 25 - 30% of the total fauna) are predators! Using a raptorial inhalant siphon, representatives of at least four families within the subclass Anomalodesmata (Parilimyidae, Verticordiidae, Poromyidae and Cuspidariidae) actively seek out and capture prey (Fig. 6) (Morton 1987) . The giant tube-worm and bivalve communities recently discovered around certain sea floor volcanic vents (such as in the Galapagos rift) also display some very unusual feeding traits . Forms such as the pogonophoran Riftia pachyptila, the vesicomyid bivalve Calytogena

390

4 Palaeoecology

Sulphide-oxidizing symbiosis in the Lucinacea . In addition to suspension-feeding, many species within this bivalve superfamily obtain nutrients from endosymbiotic bacteria . In common with other groups demonstrating this phenomenon, lucinaceans live in deep burrows; it is thought that these (or complementary tube-like structures) are essential for the accumulation of both dissolved oxygen (from surface waters) and hydrogen sulphide (from the enclosing anoxic muds) . Besides having a hypotrophied gut, lucinaceans typically display prominent ctenidia (vertical shading) which are packed full of bacteriocytes. The postero­ dorsal margins of the gills are typically fused with the muscular mantle edge and it is thought that this arrangement may facilitate the pumping of sulphide-rich waters over the bacteriocytes (especially via the exhalant siphon). Anterior foot in black . (From Reid & Brand 1986.) Fig . 7

In predatory bivalves active prey capture is achieved using an inhalant siphon which can be rapidly extended (through hydraulic pressure changes within the mantle cavity) . The siphon is retrieved (with the prey enclosed) by the action of pallial retractor muscles. Here the poromyid Poromyn grmllllntn uses a large hood at the end of the siphon to ensnare a tiny crustacean, the principal diet item of predatory bivalves . (From Morton 1987.) Fig. 6

magnifica (giant white clam), and the mytilid Bathymodiolus thermophilus are now known to be gutless . They obtain nutrients by means of endo­ symbiotic sulphide-oxidizing bacteria contained in the gill regions . These act to detoxify the sulphide­ rich volcanic waters, producing a series of carbo­ hydrates and amino acids that can then be utilized by the organisms as a food source . Similar gutless bivalves, together with forms possessing hyper­ trophied alimentary systems, have recently been shown to characterize other environments with extraordinary energy sources (such as the anoxic muds associated with marine grass beds and the effluent from fish farms and pulp mills) . Among these are shallow-water solemyid, lucinid, and thyasirid bivalves, all of which possess rich supplies of sulphide-oxidizing bacteria (Fig . 7; Reid & Brand 1986) . No longer can bivalves such as these be simply classified into either deposit- or suspension­ feeding categories . Finally, a note o f caution should b e expressed about interpreting the role of predators within palaeocommunities; in many instances it is virtually impossible to pinpoint their exact prey. Some Recent species of whelks, for example, feed on rep­ resentatives of up to eight separate phyla, and the Nassariidae (also frequently interpreted as car­ rion feeders) include at least one deposit-feeder (Ilyanassa obsoleta) . Similarly, the Cymatiidae con­ tains an algal-grazer (Apollon natator) and several

members of the Cancellariidae are probably parasitic (Taylor 1981). Clearly, the maintenance of trophic structural analysis as a viable technique in palaeoecology is going to involve the very close collaboration of palaeontologists and biologists . References Hoffman, A. 1977. Synecology of macrobenthic assemblages of the Korytnica Clays (Middle Miocene; Holy Cross Mountains, Poland) . Actn Geologica Polonica 27, 227-280 . Hoffman, A. 1979 . A consideration upon macrobenthic assemblages of the Korytnica Clays (Middle Miocene; Holy Cross Mountains, central Poland) . Acta Geologica Polonica 29, 345 - 352. Morton, B . 1987. Siphon structure and prey capture as a guide to affinities in the abyssal septibranch Anomalodesmata (Bivalvia) . Sarsia 72, 49 -69. Reid, R . G . B . & Brand, D.G. 1986. Sulfide-oxidizing symbiosis in Lucinaceans : implications for bivalve evolution. The Veliger 29, 3-24. Scott, R.W. 1976 . Trophic classification of benthic com­ munities. In : R.W. Scott & R.R. West (eds) Structure and

4. 1 7 Evolution of Communities classification of paleocommullities, pp. 29 �66. Oowden, Hutchinson & Ross, Stroudsburg, Pennsylvania. Scott, KW. 1978. Approaches to trophic analysis of paleo­ communities . Lethaia 11, 1 � 14. Stanton, R.J . , Powell, E.N. & Nelson, P.e. 1981 . The role of carnivorous gastropods in the trophic analysis of a fossil community. Malacologia 20, 451 �469 .

391

Taylor, J . O . 1981 . The evolution of predators in the Late Cretaceous and their ecological significance . In: P.L Forey (ed .) The evolving biosphere, pp. 229 �240 . British Museum (Natural History), London & Cambridge University Press, Cambridge . Walker, K.R. & Bambach, R.K. 1974. Feeding by benthic invertebrates: classification and terminology for paleo­ ecological analysis . Lethaia 7, 67�78.

4 . 17 Evolution of Communities A . J . BOUCOT

It has long been known that fossils do not occur in a random manner. Particular mixtures of taxa, with particular relative abundances, characterize every time interval and environment. These 'mixtures' may be termed communities, employing biological parlance, although some prefer the term association or assemblage. Some palaeontologists refuse to use the term community, preferring assemblage, be­ cause of the absence of soft-bodied organisms . But it is obvious that virtually all descriptions of both modern and fossil communities deal with only a small part of the total biota present, i . e . the term community commonly approximates to the definition of a guild. Thus, we have rodent communities, coral communities, brachiopod communities, trilobite communities, planktic foraminiferal communities, benthic foraminiferal communities, lichen com­ munities, larger carnivore communities, tree communities, etc. Palaeontologists and biostratigraphers of the nineteenth century did not pay much attention to what are now termed fossil communities . This probably reflects their overwhelming concern with dating and correlation of beds in which emphasis was placed on the taxa common to different collec­ tions . The study of communities emphasizes instead the taxonomic differences between collections . Only in the latter part of this century has extensive interest developed in communities, particularly because of their potential for providing a better understanding of past environments . A community may be defined as a recurring associ­

ation of taxa, in which relative taxonomic abundances remain more or less fixed. For example, brackish water

oysters remained dominant in their community from the later Mesozoic to the present, just as the brachiopod Pentamerus remained dominant in its community from the later Early Silurian to the earlier Late Silurian, and the shells in a lower dominance, later Cenozoic Pecten community retained similar relative abundance through time . The term biofacies is used in various ways (Section 4. 18) : some workers employ it when referring to what are essentially biogeographical units, such as a 'Gondwanic biofacies' ; others employ it for very broad environmental units within a biogeographical unit, such as 'deep-water biofacies' or 'black shale biofacies'; still others use it for individual com­ munity types, such as 'pentamerid biofacies', 'stringocephalid biofacies', or 'brackish water oyster biofacies' . Community evolution deals with the Darwinian species-level evolution shown by the genera present in specific community types . These narrowly de­ fined 'community types' may be referred to as com­ munity groups (Boucot 1978, 1981, 1983, 1986, 1987; Fig . 1); the term was devised to describe a com­ munity type undergoing species-level evolution among its constituent genera in evolutionary time - particularly the less abundant, commonly more endemic, and more stenotopic genera . Those who study modern communities commonly name them after the dominant, abundant taxa - those which evolve very little - whereas the changes in communities chiefly affect the uncommon genera and their rapidly evolving species. It makes sense, therefore, to name community groups after the abundant, slowly evolving genera, and the com-

392

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munities after the less common, rapidly evolving genera and their time-sequences of species . An excellent example o f community evolution was provided by Ziegler (1966), whose late Lower Silurian time sequence of species of the brachiopod Eocoelia has been well tested in eastern North America, the U.K., and Scandinavia (Boucot 1975) for nearshore, subtidal marine, level-bottom, mod­ erate turbulence, possibly turbid conditions . The

Eocoelia community, as now construed, commonly comprises more than 90% Eocoelia shells, chiefly disarticulated in a muddy matrix, and with a high population density (so-called 'pearly beds') . [Com­ munity succession, defined as the presence of one taxon making it possible for the same area to be subsequently colonized by a second taxon, is not community evolution . ] Community evolution also deals with the initial,

393

4. 1 7 Evolution of Communities quantum evolution of distinctly different, narrowly defined biofacies types from either newly evolved higher taxa or new mixtures of previously existing taxa. This phase of community evolution sees the first appearance of new community groups, and is followed by subsequent species-level changes within the initial genera, particularly, the less abundant ones. The community groups presem- within any one major subdivision (level-bottom environment, reef complex of communities, sponge forest, pe1matozoan thicket, etc . , as well as comparable non­ marine units) have concurrent times of appearance and disappearance from the base of the Cambrian to the present. These concurrent times within the level-bottom environments mark the boundaries of ecological-evolutionary units (see below) . The level-bottom community groups of the mar­ ine environment tend to be not only dominant in terms of area occupied and overall numbers of specimens per time interval, but also in strati­ graphical duration. The fossil record consists of a fixed number of time intervals, each one of which contains a relatively homogeneous biota . Boucot (1983, 1987) termed these units ecologic-evolutionary units . There are 12 such major units from the Cambrian to the present (Fig. 2) . Within marine benthic environments the level­ bottom community groups have the full time range of the appropriate ecological-evolutionary units, but the non-level-bottom community groups (reef complex communities, pelmatozoan thicket com­ munities, sponge forest communities, bryozoan thicket communities, etc.) commonly appear in time significantly later than the level-bottom groups . They do, however, commonly share the same extinction time . The reasons for relative fixity of community groups are poorly understood . They may involve a significant measure of both coevolution at one trophic level or another, and of stabilizing selection in so far as the taxa present are concerned . Biologists have not yet uncovered any very effective means of measuring levels of coevolution in modern com­ munities, although they suspect that there are major differences in levels of coevolution (viz . the coral reef community complex vs . level-bottom com­ munities, and tropical rainforests vs . grasslands) . The boundaries of ecological- evolutionary units commonly mark major extinctions followed by adaptive radiations (Boucot 1983, 1987) . Ecological ­ evolutionary subunit boundaries, such as those between the Silurian-Devonian and Mississippian-

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Pennsylvanian, are similarly marked by minor extinctions followed by minor adaptive radiations . One consequence o f community evolution at the species level is that the number of species (and genera) does not change significantly within a specific community group in any specific ecological- evolutionary unit, i . e . diversity is not in a continual state of flux. There have been many suggestions made about the factor(s) involved in extinctions (Section 2 . 1 2), but few about those controlling adaptive radiations . Major, time-concurrent, adaptive radiations within the same portion of the ecosystem affect varied, taxonomically unrelated organisms and many dif­ ferent community groups . The level of randomness involved is unknown, as is whether the presence of potentially empty niches is most important (most adaptive radiations tend to follow major extinctions) . However, the absence of the reef com­ plex of communities during many ecological ­ evolutionary units (Middle - Upper Cambrian,

4 Palaeoecology

394

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Fig. 3 A, CIa doge ne tic pattern characteristic of the organisms belonging to individual ecological -evolutionary units. Note that cladogenesis is restricted to that brief moment in time when new community groups first appear . Cladogenesis here refers to metacIadogenesis, i.e. quantum evolution mediated phenomena. Biogeographically mediated diacIadogenesis can, of course, occur anywhere within an ecological- evolutionary unit. Metacladogenesis refers to major cladogenetic events resulting in new families and higher taxa (Boucot 1978), whereas diacladogenesis refers to minor cladogenetic events giving rise merely to new genera and species, such as the post-Miocene species occurring on either side of the Isthmus of Panama. B, Cladogenetic pattern of the standard, hypothetical, random through time type, which ignores the constraints imposed by what we know about community evolution. Note that this view permits cladogenesis to occur at any time within an ecological- evolutionary unit, and is also consistent with important changes in species-level diversity within any ecological - evolutionary unit as contrasted with the conclusion outlined in A. Such random, within-unit changes in diversity do not occur . It is only by 'superimposing' family trees derived from ecologically unrelated, major parts of the global ecosystem (such as level-bottom, reef complex of communities, pelmatozoan thickets, etc . ) that one can simulate the unnatural random cladogenetic pattern . (From Boucot 1986 . )

Lower Ordovician, Famennian half of Upper Devonian, Mississippian, Lower Triassic) suggests that the empty niche possibility is incapable of explaining all the facts . Another consequence o f community evolution is that the commonly presented, hypothetical, random type of family tree (Fig. 3B) does not agree with the

more espaliered tree (Fig. 3A) indicated by species­ level evolution within community groups . This is a consequence of the fact that the community types (community groups) within each ecological ­ evolutionary unit remain relatively constant in their generic content. The evolutionary changes consist of phyletic-anagenetic changes within each genus (particularly the more stenotopic, more endemic genera, that also tend to be far less common as individual specimens) . There is not a constantly changing overall species- or genus-level diversity within either individual community groups or within major portions of the ecosystem, such as the level-bottom, during any one ecological ­ evolutionary unit. An apparently ever changing overall diversity may, however, be observed stat­ istically if disparate portions of the ecosystem are grouped together uncritically, (such as the level­ bottom, reef complex of communities, sponge forests, bryozoan thickets, pelmatozoan thickets) which commonly have different origination times within any particular ecological -evolutionary unit. References Boucot, A.J. 1975 . Evolution and extinction rate controls . Elsevier, Amsterdam. Boucot, A.J. 1978 . Community evolution and rates of clado­ genesis . Evolutionary Biology 11, 545 - 655 . Boucot, A.J. 1981 . Principles of benthic marine paleoecology. Academic Press, New York. Boucot, A.J. 1983. Does evolution take place in an ecological vacuum? 11 . Journal of Paleontology 57, 1 - 30. Boucot, A.J. 1986 . Ecostratigraphic criteria for evaluating the magnitude, character and duration of bioevents . In: O . H . Walliser (ed . ) Lecture notes i n Earth sciences, N o . 8 , pp. 25 -45. Springer-Verlag, Berlin. Boucot, A.J. 1987. Phanerozoic extinctions: how similar are they to each other? III Journadas de Paleolltologia, Leioa (Vizcaya), Palaeontology and evolution: extinction events, 50 - 82. Ziegler, A.M. 1966 . The Silurian brachiopod Eocoelia hemisphaerica (J. de C. Sowerby) and related species . Palaeontology 9 , 523 - 543.

4 . 18 Biofacies P . J . BRENCHLEY

mentally significant, but it has no value in correlation . The 'Posidonia' Shales (Section 3 . 1 1 . 6) are bitumi­ nous, laminated shales of Toarcian (Jurassic) age, widely developed throughout Germany. They are characterized by the exceptional preservation of a variety of fossils, but particularly by an abundance of the bivalve 'Posidonia' ( Bositria) . The onset of deposition of bituminous shales was apparently nearly synchronous over a wide areas and was re­ lated to the Toarcian transgression. However, depo­ sition of the shales persisted longer in basin areas than on more positive regions, so the upper bound­ ary is diachronous . The Toarcian sequence can be effectively zoned and correlated using the common ammonites, while the 'Posidonia' Shales represent a distinctive unit in that succession reflecting particu­ lar environmental conditions which determined a characteristic biota . The Wilsonia Shales (cf. Sphaerirhynchia (Wilsonia) wilsoni) are a subdivision of a generally monotonous sequence of black shales and thin laminated siltstones found at the shelf to basin transition in the Ludlow (Silurian) of the Welsh borderland . The slight vertical changes in the rather sparse fauna are more obvious in the field than any changes in lith­ ology, and it has been found useful to recognize a sequence of Cyrtoceras Mudstones, Wilsonia Shales, and Orthonota Mudstones . The Wilsonia Shales pass shelfwards into mudstones with a deep-shelf fauna and basinwards into shales containing mainly graptolites . Here we have an example of a mappable field unit comparable to a formation, but more effectively recognized on the basis of its fauna . The use of fossil names to characterize formal

Definition

The term biofacies refers to 'the total biological characteristics of a body of rock' (Moore 1949) but has been used in two rather different ways: in a stratigraphic sense to refer to 'a body of rock which is characterized by its fossil content which dis­ tinguishes it from adjacent bodies of rock', and in an ecological sense to refer to 'a biota or association of fossils which characterize a region or body of rock' .

=

Biofacies in stratigraphy

When the term 'biofacies' is used in a stratigraphic sense, the emphasis is on a geographically or verti­ cally restricted body of rock which is distinct be­ cause of its fossil content (Fig. 1 ) . The stratigraphic value of biofacies is illustrated by the widespread use of fossil names to characterize particular rock units, e . g . Pen tamer us Beds, 'Posidonia' Shales (Posidonienschiefer), and Wilsonia Shales. These three examples can be used to illustrate the role of biofacies and show how biofacies differ from biozones . The Pentamerus Beds are a varied sequence of mudstones with interbedded calcareous sandstones containing abundant Pentamerus oblongus devel­ oped in the Lower Silurian of the Welsh borderland . Pentamerus is part of an ecologically controlled community and occurred diachronously across the shelf during the Lower Silurian transgression . Thus the Pentamerus biofacies occurs locally wherever the depth, substrate, and other combination of ecologi­ cal factors were suitable . Its presence is environ-

Sea- level

Fig. 1 Distribution of five biofacies developed during a transgression. Note that biofacies 1 and 2 coincide with lithofacies, but that biofacies 3, 4, and 5 are developed within a single mud lithofacies .

D WAmid

5 4 3 2

MUd Silt Sand

395

4 Palaeoecology

396

lithostratigraphic units is now deemed invalid and most of the 'biofacies' have either been redefined as formations based on their total litho logical and bio­ logical characteristics, or have become obsolete . Particularly distinctive biofacies will, however, probably persist in the literature as informal units . Ecological use of biofacies

The term 'biofacies' in an ecological and environ­ mental sense is usually used to express the lateral or vertical variation in biota in relation to differences in environment. For example, trilobite biofacies in the Cambrian of the western U . S . A . have been de­ scribed in terms of their environmental position, i . e . inner shelf, outer shelf and slope . Biofacies have also been applied in an even more general sense to express broad lateral changes in biota according to environment. Thus, House (1975) described the marine Devonian of Europe in terms of biofacies regimes which represent the characteristic Devonian faunas of the near shore, shelf, and basinal regions . In a more detailed biofacies analysis of Ordovician rocks in the Upper Mississippi Valley, U . 5 . A . , factor analysis was used to define seven faunas distributed over 65 000 km2 of outcrop within a single member (the Mifflin Member of the Platteville Formation) . Each of these bivalve/brachiopod faunas differed and their geographical occurrence could be mapped to show biofacies distributions in an extensive, shallow epeiric sea (Bretsky et al. 1977) .

M)N::;jj

t8 § �

One of the valuable facets of the term 'biofacies' is that it can be applied to faunal associations iden­ tified with very different degrees of taxonomic pre­ cision. In some environmental studies it may be important to define the associations by the assem­ blages of species, but in other situations a very broad characterization of the fauna, such as 'coral! brachiopod association', may be appropriate . Terms commonly used in palaeoecology which are closely related to biofacies are: faunal association, community, palaeocommunity, and benthic assemblage. The first three of these terms attempt to express a distinct association of taxa which probably lived together. The regional distribution of faunal as­ sociations or communities on the sea floor or in a body of rock can be referred to as a 'biofacies' . For example, Bretsky (1969) described three com­ munities, the Sowerbyella- Onniella community, the Orthorhynchula-Ambonychia community, and the Zygospira-Hebertella community, from Upper Ordovician rocks of the Central Appalachians . The communities were recognized as distinct associ­ ations of taxa, and the geographical distribution of such communities can be shown on a biofacies map (Fig. 2) . The term benthic assemblage has been used by Boucot (1975) to identify communities which lived in the same position relative to the shoreline . Benthic assemblages are therefore approximately depth related, although temperature, substrate, and other ecological controls may be important in deter-

S a n dston e S i ltsto n e shale L i m e st o n e

Fig. 2 Biofacies map of Upper Ordovician community distribution in the Central Appalachian region, U.S.A. 1 Sowerbyella- Onniella community, 2 Orthorhynchula- Ambonychia community, 3 Zygospira- Hebertella community, 4 offshore faunas . (After Bretsky 1969 . ) =

=

=

=

4 . 1 8 Biofacies mining their location . Boucot identified six benthic assemblages in his treatment of Silurian -Devonian communities . According to Boucot, nearshore and inner shelf faunas can be referred to benthic assem­ blages 1 and 2, mid-shelf faunas to benthic assem­ blages 3 and 4, and outer shelf and upper slope faunas to benthic assemblages 5 and 6 (Fig. 3) . Faunas of quite different ages can be assigned to the same benthic assemblage because they have the same range of fossil groups though the taxonomic composition is different in detail. Such a similarity of faunas was recognized in nearshore carbonate communities of Ordovician and Devonian age and was characterized as congruent communities . They could equally well have been characterized as eco­ logical stable biofacies . This usage has been applied to the persistent community found in dysaerobic sediments of Middle Devonian - Early Permian age, which has been referred to as the dysaerobic biofacies (Section 4 . 19.4) .

397

Recent biofacies

The concept of biofacies draws strength from studies of modern benthic faunas . Petersen (1915), using grab samples in Danish waters, showed that there were areas of the sea floor characterized by particu­ lar associations of bivalve, echinoid, and polychaete worm species . The distribution of these level­ bottom communities is approximately related to distance offshore and depth of water, and hence it is possible to map out approximately shore-parallel biofacies . In general, ecological zonation of faunas on level-bottom shelves is relatively simple because: (1) there is an absence of dense flora, and hence the communities are principally influenced by physico­ chemical aspects of the environment and biotic interactions amongst members of the community; (2) level-bottoms lack micro-landscape and are environmentally relatively homogeneous, so the faunal associations occupy a single habitat rather

Q u iet water

·: : �:·:·::"·: m '; .;:. : : : : : . ::0.:.:.:.:; : :°:°

I n te r m ed iate R o u g h water

Relationship between Silurian epifaunal benthic assemblages and communities . Three possible applications of the term 'biofacies' are shown. A, Term refers to rocks containing a particular community. B, Term refers to all nearshore communities . C, Term refers to rocks containing a group of communities with some taxonomic similarities . (After Boucot 1975 . ) Fig. 3

398

4 Palaeoecology

than a mosaic of micro-habitats; (3) substrate type approximately reflects the hydrodynamic conditions of the area and is often roughly correlated with several physico-chemical parameters, such as tur­ bidity, mobility of substrate, oxygen, and organic content; (4) a large proportion of level-bottom dwelling animals are suspension feeders and the trophic structure is relatively simple (Thorson 1971 ) . I t has been claimed b y Thorson that level-bottom communities which occupy approximately the same position relative to shore (e .g. belong to the same benthic assemblage) have a similar appearance wherever they are found in the world . These belts of similar communities, with different species but sharing some genera were termed parallel

communities . Communities which inhabit rocky shorelines and to a lesser extent carbonate-producing regions have a much more complex and patchy distribution . Although there is a general shore-parallel distri­ bution of communities in carbonate regions, local heterogeneity of the sea floor, particularly where reefs are present, produces a mosaic pattern of biofacies on a local scale . Biofacies distribution

Most marine biofacies are broadly related to water depth and sediment substrate, but other physico­ chemical parameters, such as availability of oxygen, salinity, or substrate mobility may modify any sim­ ple distribution pattern . Biofacies which are pre­ served in adjacent positions in vertical sequence are believed to have generally occupied adjacent pos­ itions on the sea floor and therefore behave in a similar manner to lithofacies, according to Walther's Law . At any one time, biofacies distribution, re­ flecting the community distribution of that time, will be somewhat different in different faunal prov­ inces, particularly if they belong to different climatic belts . In general, biofacies have a greater biomass and are more diverse in tropical than arctic regions, and tropical carbonate shelves are probably par­ titioned into more biofacies than are clastic shelves in cold er regions . In any one faunal province, biofacies generally show distinct changes in taxonomic diversity and biomass in any onshore to offshore transect . In modem environments, biofacies generally decline in biomass towards the deeper parts of the shelf and then rapidly down the continental slope . Diver­ sity is usually low in any one nearshore environ­ ment, but because of the large number of nearshore

environments the total diversity of the nearshore region can be high . Diversity is relatively high across the continental shelves and can remain moderately high to the base of the slope, to depths as great as 4000 m. The pattern of onshore - offshore change in different for different parts of geological history, as will be described below. Biofacies distribution in the Phanerozoic

Cambrian biofacies . On Cambrian clastic shelves bio­ facies containing trilobites, inarticulate brachio­ pods, and molluscs are rather poorly differentiated and no clear onshore - offshore trends have been defined . The very diverse, mainly soft-bodied, Middle Cambrian, Burgess Shale fauna of British Columbia (Section 3 . 1 1 . 2) is evidence that Cambrian faunas were far richer than is suggested by the shelly assemblages, and that ecological zonation may have been more refined than is recorded by the commonly preserved fossils . In carbonate shelf and slope environments of the western U . S . A . a clear differentiation has been rec­ ognized between trilobite faunas living on the plat­ form and shelf edge (Hungaia fauna) and a trilobite fauna which occupied deeper-water sites (Hedinaspis fauna) . Ordovician and Silurian biofacies. Following the ex­ tinction of a substantial part of the Cambrian fauna, there was a major radiation in Early Ordovician times which produced a varied benthic fauna of suspension-feeding animals with skeletons . These suspension-feeding faunas became partitioned into a number of biofacies, approximately related to water depth, in the early part of the Ordovician. Progressively during the Early and Middle Ordovician there was colonization of the deeper parts of the shelves (Sepkoski & Sheehan 1983) . This established a pattern where about five or six communities (biofacies) occurred in any transect across a level-bottom clastic shelf in the later Ordovician and Silurian (see Fig. 3) . The communi­ ties were generally brachiopod-dominated, but bryozoa, corals, and crinoids were also important elements, and trilobites and bivalves were often associated with the fauna (McKerrow 1978) . Nearshore biofacies typically had a low species diversity and a very variable biomass which could be high when environmental conditions were favourable . The faunas were characterized by ar­ ticulate brachiopods, particularly large orthids,

4 . 1 8 Biofacies bivalves, and sometimes inarticulate brachiopods such as Lingula. Along a traverse outwards across the shelf there was a general increase in taxonomic diversity towards the shelf margin, though there could be local areas of particularly high diversity in mid-shelf regions where carbonate build-ups de­ veloped . Abundance of fossils and total biomass was generally high into mid-shelf regions, but de­ creased towards the outer shelf and declined very rapidly down the slopes . The exact patterns of di­ versity and biomass depended on the depth of the shelf- slope break and the influence of other limiting factors, such as oxygen. Typical mid-shelf biofades in the Silurian have diverse brachiopod faunas with pentamerids, atrypids, strophomenids, and orthids, with variable numbers of associated bryozoa, tabulate and rugose corals, crinoids, and

399

trilobites . In biofacies of greater shelf depths, tabu­ late corals, bryozoa, and crinoids are rarer, trilobites are relatively more important, and the brachiopod fauna, though still diverse, is commonly composed of relatively small-shelled forms . At the shelf edge the diversity and abundance of the brachiopod fauna declines sharply, and slope faunas are usually sparse with some trilobites and molluscs (and rela­ tively more pelagic elements) with increasing depth . This pattern of biofacies applies to clastic shelves in temperate regions . Diversity and biomass were generally lower in colder regions where there were fewer communities and the shelf was partitioned into fewer biofacies . In contrast, carbonate fades of tropical regions had very diverse faunas and a large biomass . Carbonate environments on broad epeiric platforms were often very extensive in the Lower

A (10

1 00 '" c .2 75 Cl..

L.U

50 25

c

'" 60

.2 40 c

20

B

Mean d iversity

A, Diagram to show the relative abundance of epifaunal and infaunal bivalves according to type of substrate in the Corallian. B, Diversity indices (using rarefaction method at 60 individual levels) of the macroinvertebrates in different substrates . 1 condensed limestone, 2 condensed ferruginous sediments, 3 patch reefs, 4 clays, 5 silts, 6 fine sand, 7 medium- coarse sand, 8 oolites, 9 fine-grained limestone, 10 coarse-grained limestone. Note diversity change between clays (4) and coarse sand (7) . (After Flirsich 1976 . ) Fig. 4

24

20 16

=

=

12 -

=

=

=

=

=

=

8

=

=

4

400

4 Palaeoecology

Palaeozoic, giving rise to regionally developed bio­ facies . However, in areas where reefs were developed, the biofacies could be very patchy.

Upper Palaeozoic biojacies. The broad patterns of diversity and abundance established in the Lower Palaeozoic were probably continued into the Upper Palaeozoic. The largest changes in the appearance of biofacies arose from the increasing importance of terebratulid and productid brachiopods . There was a significant change in Devonian biofacies caused by the Late Frasnian extinction (Section 2 . 13 . 3) of the Pentameridea, Atrypoidea, and Orthacea and the subsequent enrichment of the rhynchonellid and productid faunas (McKerrow 1978) . Mesozoic biojacies. The end-Permian mass extinction (Section 2 . 1 3 .4) destroyed the major part of the Palaeozoic benthic associations and new faunal as­ sociations established themselves in the Triassic. Mesozoic biofacies are generally dominated by bi­ valves with variable proportions of gastropods, brachiopods, echinoids, crinoids, and corals . The partitioning of level-bottom shelves into belts oc­ cupied by distinct benthic assemblages has not been clearly demonstrated in the Mesozoic, although there are obvious changes in faunal com­ position with increasing water depth . There is gen­ erally a correlation between taxonomic composition and substrate but, because some bivalves are eury­ topic, this correlation is not always pronounced. A detailed study of Corallian (Jurassic) palaeoecology (Fiirsich 1976) recognized 17 faunal associations oc­ cupying a range of environmental situations from nearshore to open shelf. Some of these associations showed a close correlation with substrate, others little or no such correlation. In general, deposit­ feeding bivalves had a preference for fine silts or argillaceous silts, but avoided clays; epifaunal sus­ pension feeders dominated condensed facies and patch reefs but avoided soft clay substrates; and infaunal suspension feeders were particularly com­ mon in clay substrates (Fig. 4) . Mean diversities of the fauna were high in condensed facies and clays, and generally showed a marked decrease in diver­ sity with increasing grain size (Fig. 4) . This diver­ sity- grain size relationship was interpreted to reflect an increasing environmental instability in

more energetic nearshore environments relative to the more stable offshore regions . Tertiary to Recent. The end-Cretaceous extinction (Section 2 . 1 3 . 6) modified the Mesozoic biota by the loss of ammonites, belemnites, inoceramid and rudist bivalves, and several groups of gastropods . In addition, the abundance of brachiopods was reduced and many echinoid taxa disappeared . Several groups which were often present i n the Cretaceous, but in subordinate proportions, diver­ sified in the Early Tertiary; predatory gastropods, Neogastropoda, polychaete worms, heterodont bi­ valves, the Veneracea, and Tellinacea all probably diversified at this time . Reef-building corals and associated algae also apparently diversified in the Eocene . Typical Tertiary biofacies are dominated by bivalves and gastropods, and from Miocene times had a taxonomic composition, at generic level, similar to biofacies found in the Recent. References Boucot, A. 1975 . Evolution and extinction rate controls. Elsevier, Amsterdam, Oxford. Bretsky, P.W. 1969 . Central Appalachian Late Ordovician communities . Bulletin of the Geological Society of America 80 , 193-212. Bretsky, P.W., Bretsky, S5. & Schaefer, P.J. 1977. Molluscan and brachiopod dominated biofacies in the Platteville Formation (Middle Ordovician), Upper Mississippi Valley. Bulletin of the Geological Society of Denmark 26, 1 1 5 - 132. Fiirsich, F.T. 1976 . Fauna - substrate relationships in the Corallian of England and Normandy. Lethaia 9, 343 - 356. House, M.R. 1 975. Faunas and time in the marine Devonian. Proceedings of the Yorkshire Geological Society 40, 459 -490 . McKerrow, W5. (ed . ) 1978. The ecology offossils . M.LT. Press, Cambridge, Ma. Moore, R.C 1949 . Meaning of facies . Memoirs of the Geological Society of America 38, 1 - 34 . Petersen, C C .J . 1 9 1 5 . O n the animal communities o f the sea bottom in the Skagerrak, the Christiana Fjord and the Danish waters. Report of the Danish Biological Station 23, 3-28. Sepkoski, J .J . , Jr. & Sheehan, P.M. 1983. Diversification, faunal change and community replacement during the Ordovician radiations . In: M.J5. Tevesz & P.L. McCall (eds) Biotic interactions in Recent and fossil benthic communities, pp. 673 - 717. Plenum, New York. Thorson, G. 1971 . Life in the sea . Weidenfeld and Nicholson, London.

4 . 19 Fossils as Environmental Indicators

4 . 19 . 1 Climate from Plants

Leaf margins. In modern vegetation the ratio of non­ entire (toothed) to entire (smooth) margined leaves correlates strongly with mean annual temperature (MAT) (Wolfe 1979; Fig. 2) . Generally, in the North­ ern Hemisphere a change of 3% in this ratio corre­ sponds to a change in MAT of 1°C. In the Southern hemisphere, with a higher proportion of evergreen taxa, a 4% change corresponds to 1°C . Because major tooth types had evolved by the Cenomanian, and because Cenomanian leaf margin ratios cor­ relate with palaeolatitude, this technique seems applicable from the early Late Cretaceous to the present. A minimum of 20 leaf species are required at any one locality to make this technique reliable, and taphonomic factors have to be taken into consideration.

R. A . SPICER

Vegetational physiognomy

Vegetation, unlike marine organisms, is directly exposed to the atmosphere . The physiognomy (structure and composition) of environmentally equilibrated (climax) vegetation is in large part con­ trolled by, and therefore reflects, climate (Wolfe 1979) . Interpretations of climate based on veg­ etational physiognomy, foliar physiognomy, or wood anatomy are more reliable for pre-Neogene studies than taxon-dependent climate signals (those used in Nearest Living Relative - NLR methods) . Fundamental vegetational types can be recognized in modern vegetation and, provided water is not limiting, correlate with temperature regimes (Fig. 1 ) . These vegetational types can be recognized with some confidence back to late Cretaceous (Cenomanian) times .

Leaf size. This is related strongly to temperature, humidity/water availability, and light levels . Large leaves occur in humid understories, and size decreases with decreasing temperature or precipi­ tation. Size classes are used to characterize veg­ etational types and to construct leaf size indices (which are used to characterize overall leaf size parameters for a given vegetational type) . In fossil assemblages leaf size suffers strong taphonomic bias.

Features o f leaves useful in determining palaeoc1imate

Angiosperm vegetative organs exhibit considerable morphological diversity and flexibility with respect to climate . The following features are those of angiosperms except where indicated:

Drip tips. Highly attenuated leaf apices occur most frequently in evergreen leaves in humid environ­ ments, and are particularly common in the under­ storey of multistratal rain forests . Drip tips may

30 �

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Correlation of fundamental vegetational types with temperature regimes . Fig. 1

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Palaeoecology

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Fig. 2

enhance drainage of surface water from the leaf and thus retard the growth of epiphytes .

2).

Leaf texture. Leathery (coriaceous) leaves typically are evergreen and predominate in megathermal and mesothermal vegetation (see Fig. Thin (char­ taceous) leaves are typically deciduous and are most common in micro thermal climax or successional mesothermal vegetation .

Leaf shape. Stream-side vegetation contains a high proportion of narrow (stenophyllous) leaves. Lobed or compound leaves (also associated with decidu­ ousness) occur with greatest frequency in suc­ cessional vegetation or under storey communities, and therefore warn of bias in the climate signal. Thick cylindrical leaves in any plant group are evi­ dence of aridity, growth in saline water, or an inefficient vascular system .

Leaf cu tides. In all terrestrial plant groups thick cuticles with numerous trichomes (hairs) are characteristic of plants adapted to desiccating con­ ditions (drought or salinity) . Sunken stomata, par­ ticularly if overarched by papillae, and low stomatal density are also indicative of water stress . Con­ versely, thin, smooth cuticles suggest water-rich conditions . Wood anatomy

Manoxylic (parenchymatous) wood (e . g . modern relict cycads) is frost-sensitive, while pycnoxylic (mostly composed of secondary xylem) wood (coni­ fers and angiosperms) is usually frost-resistant.

Tree rings. In situations where climatic conditions

vary frequently, pycnoxylic wood produces rings as a consequence of variations in growth rate . Rings may be produced on an annual basis where tem­ perature, light, or water availability fluctuates on a yearly cycle, or less regularly in environments with more erratic variations in growth conditions (e .g. sporadic droughts) . Annual rings consist of early (spring) wood with large cell lumina and thin cell walls that grade into late (summer) wood, in which the lumina are smaller and the walls thicker. Wide rings generally reflect benign conditions, but ring width is also a function of position within the tree (position within the trunk, or trunk versus branch) (Creber & Chaloner 1985) . High early wood - late wood ratios indicate a high rate of spring and summer growth followed by rapid onset of dormancy . At high latitudes this may be controlled by light rather than temperature . Inter-annual variations in ring width are de­ scribed using a statistic known as mean sensitivity:

XI

ms

1

=

-

n

1

12(XIXI+1+ 1 - XIXI) I , Xt+ 1

,, 1 = ,, - 1 L... 1= 1

+

where is a ring width, is the width of the adjacent younger ring, and n is the number of rings so measured in a sequence . Woods with a mean sensitivity of < 0.3 are termed complacent and in­ dicate uniform growing conditions from year to year. Sensitive woods (ms > 0.3) are typical of trees growing at the edge of their range and/or in vari­ able environments . Intra-annual variation is marked by false rings . Unlike true rings these often do not form complete circles as seen in cross-section, and may be gra­ dational to normal (usually early) wood on both concave and convex sides . False rings reflect tem­ porary trauma within the growing season caused by waterlogging of roots, low temperatures, or severe insect attack, for example . Frost rings are characterized by cell wall disruption due to freezing of cell contents . Pycnoxylic wood is known from the Late Devonian to the present. In angiosperm woods average vessel diameter divided by the frequency of vessels per mm2 in cross-section estimates the susceptibility of a tree to air embolism (formation of air bubbles and damage to conductive elements) caused by transpirational stress or freezing . As with leaves, the reliability of the climate signal in wood increases with sample size and taphonomic understanding .

4 . 1 9 Fossils as Environmental Indicators NLR methods Plant reproductive organs have little inherent cli­ matic signal but climate may be deduced from extra­ polation of the tolerances of their NLRs . Following Axelrod & Bailey (1969), four steps are required in NLR analysis : 1

NLR o f all taxa i n a n assemblage should be identified to modem genus level. 2 NLR determinations should also be attempted at species level (because generic tolerances are too broad) . 3 The average MAT and average mean annual range of temperature (MAR) are estimated based on habit 'preferences' of modem NLRs . 4 The effective temperature (average temperature at the beginning and end of a period free from frost or chill) and equability of the palaeoclimate are calculated using the average MAT and MAR.

References Axelrod, DJ. & Bailey, H.P. 1969. Paleotemperature analysis of Tertiary floras. Palaeogeography, Palaeoclimatology, Palaeoecology 6, 163- 195. Creber, G.T. & Chaloner, W.G. 1985 . Tree growth in the Mesozoic and early Tertiary and the reconstruction of palaeoclimates . Palaeogeography, Palaeoclimatology, Palaeoecology 52, 35-60. Wolfe, ].A. 1979 . Temperature parameters of humid to mesic forests of eastern Asia and their relation to forests of other areas of the Northern Hemisphere and Australasia, US Geological Survey Professional Paper No . 1 106.

4.19.2 Temperature from Oxygen Isotope Ratios T . F . ANDERSON

Introduction

Oxygen isotope ratios e80 : 160) of well preserved marine calcareous fossils are indicative of the tem­ perature of ancient ocean waters . This approach is based on the fact that the difference in 180 : 160

403

ratios between calcium carbonate and the water from which it precipitates is a function of tempera­ ture . Oxygen isotope ratios are expressed in the 0 notation :

Units are per mil or parts per thousand . The standard material for carbonates is PDB, a late Cretaceous belemnite from the Pee Dee Formation of South Carolina; for water, the standard is SMOW, i . e . standard mean ocean water (see Anderson & Arthur 1983) . Oxygen isotope palaeotemperatures for calcite can be calculated from: TOC

=

16.0 - 4 . 14� + 0 . 13� 2,

(2)

where � 0180 calcite (vs . PDB) - 0180 water (vs . SMOW) (Anderson & Arthur 1983) . Thus, 0180 of calcite increases as temperature decreases . Palaeo­ temperature estimates can be made with an uncer­ tainty of ± O . soC, because 0180 values are measured to a precision of 0 . 1 per mil . Factors other than analytical precision control the uncertainty in isotopic palaeotemperatures : 1 The manner in which isotopic fractionation be­ tween biogenic calcium carbonate and water varies with temperature must be known . Equation (2) applies to inorganic precipitation of pure calcite at isotopic equilibrium and to a number of low­ magnesium calcite fossil groups including bivalves, belemnites, brachiopods, and planktic foramini­ fera. Slightly different equations apply to preserved aragonite and high-magnesium calcite shells (Anderson & Arthur 1983) . In addition, physio­ logical effects during shell secretion in some organisms result in departures from equilibrium fractionation; notable examples are corals and echinoids . 2 I t i s necessary to estimate the 0180 o f the water in which the shell grew. In the hydrologic cycle, evap­ oration preferentially removes H2160 from water, while precipitation and runoff returns H2160. Local variation in the hydrologic balance of ocean waters of normal salinity can produce small variations in 0180. (The range for modem seawater is 2.S per mil . ) This effect i s normally ignored in estimating isotopic palaeotemperatures because hydrologic data on ancient ocean water is lacking. Also, because H2160 is preferentially stored in polar icecaps and conti­ nental ice sheets, oceans are enriched in 180 during glacial epochs relative to nonglacial epochs. For example, the growth and decay of continental ice =

404

4 Palaeoecology

sheets during the Late Quaternary produced excur­ sions of at least 1 per mil between glacial and inter­ glacial oceans . The effect of Palaeozoic glaciations on the 0180 of contemporaneous seawater was probably similar. 3 Reliable isotopic palaeotemperatures can be obtained only from those fossils that have been preserved from diagenetic alteration . Cemented or partially recrystallized fossils will generally give er­ roneous palaeotemperatures, because secondary carbonates reflect the temperature and isotopic composition of diagenetic solutions . Isotopic palaeotemperatures from the Cenozoic and Late Cretaceous

The most continuous record of marine temperature variations for the past 100 million years has been constructed from isotopic analyses of well preserved foraminifera in deep-sea sediments . Diagenetic alteration of foraminiferal tests is minor and rela­ tively easy to determine microscopically. In ad­ dition, the effects of continents on the temperature and 0180 of ocean water in the pelagic realm is minimal. The Quaternary oxygen isotope record of fora­ minifera shows oscillations with periods of about 10 5 years between 0180 maxima during glacials and 0180 minima during interglacials (see Savin 1977, fig . 8; Anderson & Arthur 1983) . Although the direction of these isotope shifts is qualitatively compatible with temperature changes, it is now generally accepted that the amplitude of Quaternary 0180 oscillation reflects changes in continental ice volumes more than changes in seawater temperatures .

0

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Marine temperatures for the Tertiary and Late Cretaceous have been estimated from isotopic data on Deep Sea Drilling Project cores. Composite oxygen isotope records for planktic and benthic foraminifera from subtropical sites in the North Pacific illustrate the major features of palaeoclimatic changes over the past 130 million years (Fig. 1 ) . The planktic record reflects temperature and 0180 vari­ ations in low-latitude surface waters; the benthic record reflects conditions at the high-latitude source regions of deep-water masses. The data suggest general cooling in the Pacific over the past 100 million years . Temperatures of subtropical surface waters were evidently warmer in the Albianl Cenomanian and the Eocene than in intervening times . Temperature trends in deep waters are cor­ related with those of surface waters from the Middle Cretaceous through the Early Tertiary. However, bottom waters during this interval (especially during the Cretaceous) were considerably warmer than at present. In other words, the latitudinal con­ trast in ocean temperatures had increased during the Tertiary, resulting principally from apparent cooling at high latitudes. Abrupt positive shifts in the Tertiary benthic 0180 trend probably reflect the initiation (Eocene - Oligocene) and rapid expansion (Middle Miocene) of the Antarctic icecap, as well as a decrease in high latitude surface temperatures . Palaeotemperature trends from shallow-marine bivalves from northwest Europe (Fig. 2) are similar to those for Pacific low-latitude surface waters (Fig. 1), suggesting that global palaeodimatic changes were not obscured by the influence of continents on the temperature and 0180 of nearshore seawater. In contrast to the deep-sea record, the isotopic data from bivalves suggest that the shallow

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405

4 . 1 9 Fossils as Environmental Indicators Alb

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Isotopic palaeotemperatures from the Palaeozoic

Isotopic palaeotemperature de terminations on Palaeozoic fauna are limited necessarily to shallow­ marine taxa . The most serious problem with Palaeozoic fossils is the preservation of the original isotopic signal through early diagenesis and long­ term burial. Several recent studies have suggested that trace element compositions and microscopic textural characteristics can be used to identify iso­ topic preservation in fossil brachiopods (Popp et al. 1986; Veizer et al. 1986) . Specifically, portions of

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brachiopods which are not cathode luminescent and whole brachiopod shells with low Mn and Fe contents have probably suffered only minimum dia­ genetic alteration . Data on well-preserved brachio­ pods from a range of locations, supplemented with estimates for primary marine cements, indicate that 6180 values increased irregularly during the Palaeozoic, with a major positive shift from the Devonian to the Carboniferous (Fig . 3) . The extent to which this and similar 6180 age trends for cherts and sedimentary phosphates represent decreasing temperatures or increasing 6180 of ocean water is a major controversy in stable isotope geochemistry. The resolution of this controversy will have a pro­ found impact on our interpretation of surface tem­ perature variations and hydrosphere - lithosphere interactions through time (Anderson & Arthur 1983; Veizer et al . 1986) .

4 Palaeoecology

406 References

Anderson, T.F. & Arthur, M.A. 1983 . Stable isotopes of oxygen and carbon and their application to sedimentologic and paleoenvironmental problems . In: Stable isotopes in sedi­ mentary geology, SEPM Short Course Notes No . 10. Society of Economic Paleontologists and Mineralogists, Tulsa. Buchardt, B. 1977. Oxygen isotope palaeotemperatures from the Tertiary period in the North Sea area. Nature 275, 121 - 123. Popp, B . N . , Anderson, T.F. & Sandberg, P.A. 1986. Brachio­ pods as indicators of original isotopic compositions in some Paleozoic limestones . Bulletin of the Geological Society of America 97, 1262- 1269 . Savin, S.M. 1977. The history of the Earth's surface tempera­ ture during the last 100 million years. Annual Review of Earth and Planetary Sciences 5, 319-355 . Veizer, J . , Fritz, P. & Jones, B. 1986. Geochemistry of brachio­ pods : oxygen and carbon isotopic records of Paleozoic oceans. Geochimica et Cosmochimica Acta SO, 1679- 1696.

4 . 19 . 3 Salinity from Faunal Analysis and Geochemistry J . D . HUDSON

Introduction Salinity is one of the main controls on the clistribution of the aquatic biota, and the estimation of palaeosalinities has concerned many palaeoecol­ ogists. Most work has involved benthic invert­ ebrates with calcium carbonate hard parts, although palynology has important applications . Fossil oc­ currences of particular taxa or assemblages may be compared to modem distributions . Alternatively, fossils can be analysed geochemically, as convenient samplers of the waters they inhabited. Sediment­ ological evidence also should be sought. The usual result of such studies is an empirical estimate of the palaeosalinity, or range of salinities, experienced by the organisms, and is generally ex­ pressed in parts per thousand or in the 'Venice System' (Fig . 1 ) . The recognition of fully-marine faunas is generally not controversial; nor, in Meso­ zoic and Cenozoic rocks, is that of freshwater lake faunas . Most palaeoenvironmental interest thus centres on the brackish water and hypersaline faunas of estuaries and other coastal environments, and of saline lakes. Most brackish systems are labile, and the range and rate of salinity change may have as great an

effect as mean salinity. Water boclies whose salinity varies are commonly also variable in temperature, depth, food supply, etc . , and are often underlain by soft, organic-rich substrates . Therefore effects on biotic distribution caused directly by salinity are hard to disentangle from those which are due to other controlling factors . Besides palaeoenvironmental interpretation, more fundamental questions concern: the mechan­ ism(s) by which salinity control operates; whether there is a special brackish water fauna as opposed to merely a reduced-marine one; the evolutionary origin of brackish water faunas; and the relationship of brackish water faunas to the invasion of fresh­ waters or land by various groups of organisms . On the long time-scale, there is also the possibility that the composition of seawater itself may have changed . Palaeontology supplies essential historical data bearing on these biological and geochemical questions .

Faunal analysis The normal palaeoecological precautions about working with in situ assemblages obviously apply; in particular, because salinity in estuaries and la­ goons can vary so rapidly, the importance of finely­ controlled collecting cannot be overstressed . Even so, some time-averaging of fine-scale variation inevitably occurs . Many higher taxa of plants and animals today are effectively marine-stenohaline and their occurrence, especially in combination, can be used to infer fully marine salinity: viz. corals, cephalopods, echino­ derms, bryozoans, articulate brachiopods, planktic and larger benthic foraminifera, and many cal­ careous red and green algae . Most of these, however, include some partially euryhaline forms extending into polyhaline waters . Only a small number of higher taxa thus account for most of the modern brackish and freshwater shelled fauna, i . e . bivalves, gastropods, ostracodes, smaller benthic foraminifera, and charophyte algae . Non-calcified arthropods are important but seldom preserved except as trace fossils (conchostracans being an exception) . Many 'fish' are and have been euryhaline, although often also migratory and subject to vagaries of preser­ vation . Even among these groups, few lower taxa have given rise to genera or species tolerant of mesohaline or more dilute waters . Most freshwater taxa are strictly stenohaline . It follows from these considerations that brackish and freshwater faunas are of low taxonomic diver-

4 . 1 9 Fossils as Environmental Indicators

407 ...

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sity and comprise distinctive taxa . Few taxa are specifically adapted to brackish water and most of these are not normally capable of fossilization. They occur along with the more euryhaline members of the marine fauna and in mesohaline waters the latter generally dominate . A few freshwater forms penetrate oligohaline waters . Thus the diversity minimum is generally identified at 5 - 90/00 salinity, as first recognized by Remane in the Baltic Sea (Fig. 1 ) . The reasons for this minimum have been much debated. It now appears that it does not correspond to a particularly sharp change in ionic ratios in most estuarine or lagoonal settings . A change from (Na + , Cl-) to (Ca2+ , HC03 -) dominated chemistry does, however, occur in more dilute waters in some areas and creates a sharp distinction between marine­ derived brackish and non-marine ostracode faunas (Forester & Brouwers 1985) . In inland lakes, ionic ratios, more than total salinity, control ostracode distributions (Forester & Brouwers 1983) . Brackish waters are often very productive because nutrients introduced from the land and estuarine circulation, with inflow of enriched subsurface sea­ water, can turn estuaries into nutrient traps . This combination of high fertility with physiological stress gives brackish water faunas their well known character of containing few species but many indi­ viduals . The species tend to be morphologically 'generalized' and the individuals small. This is both because the species are opportunists, r-selected for

rapid exploitation of unstable resources and there­ fore commonly of small adult size, and because populations may contain many juveniles . The faunas o f hypersaline lagoons have some similarities to those of brackish lagoons, and the same major groups are involved . However, the lower taxa are generally different (e . g . miliolid rather than rotaliid foraminifera), and so are the sedimentary facies associations . Saline continental lakes may have different chemistry from seawater and have special faunas . Large inland seas of marine origin, such as the Caspian Sea, are also special cases.

Geochemistry The trace element content of carbonate and phos­ phate shells must be related to that of the water their bearers inhabited, but there are many chemi­ cal, physiological, and diagenetic complications in applying this relationship in fossils . Relationships between the strontium : calcium ratio, for example, and salinity have been established for particular marine taxa and regions, but cannot as yet be gen­ eralized . In simple lacustrine settings the strontium: calcium ratio of ostracode shells correlates with salinity (Chivas et al . 1985) . The distribution of the stable isotopes of carbon and oxygen, while also not free of complications, has been of more general utility (Dodd & Stanton 1981) . The 1 80 : 160 ratio in seawater has been rather constant ( 0 1 80SMOW =

408

4 Palaeoecology

- 1 to 0%0; Section 4 . 19.2), at least since the Late Palaeozoic. Meteoric water is variably 180 depleted (6180 - 3%0 in the humid sub-tropics, -50%0 in polar ice) . Dissolved bicarbonate in seawater is rela­ tively 13C rich (613CPDB 0 to 30/(0); river and lake bicarbonate generally contains carbon derived from the oxidation of plant material, and is thus variably -5 to - 12%0) . In a simple river 1 2C enriched (613C estuary, therefore, salinity, 6180, and 613C are all linearly correlated, and the isotopic variations are reflected in the shells of molluscs living along the estuary (Mook 1971 ) . (Temperature also affects 6180, as discussed in Section 4 . 19.2, but seawater ­ freshwater mixing in a small area generally out­ weighs the temperature effect. ) These principles can b e applied to well-preserved fossils . The best criterion of isotopic preservation is the retention of original aragonite in molluscs . Complications include the fact that 6180 can be increased by evaporation of freshwater as well as by mixing, so that low-salinity water can attain positive 6180 values, as in the Florida Everglades (Uoyd 1964) . Humid-region lakes generally have negative 6180 and 613C values in fossils; arid-zone lakes can be variable in both ratios . Especially in the Palaeo­ zoic, time-related changes have occurred in the 613C and 6180 of even fully-marine carbonates, making salinity-related changes harder to detect. =

=

=

References Chivas, A.R., De Deckker, P. & Shelley, M . G . 1985 . Strontium content of ostracods indicates lacustrine palaeosalinity. Nature 316, 251 - 253 . Dodd, J.R. & Stanton, R.J . , Jr. 1981 . Palaeoecology, concepts and applications . J. Wiley & Sons, Chichester. Forester, R M . & Brouwers, E.M. 1983 . Relationship of two lacustrine ostracode species to solute composition and salinity: implications for paleohydrochemistry. Geology 11, 435 -438. Forester, R.M. & Brouwers, E.M. 1985 . Hydrochemical par­ ameters governing the occurrence of estuarine and mar­ ginal estuarine ostracodes : an example from south-central Alaska . Journal of Paleontology 59, 344 - 369. Fiirsich, F.T. & Werner, W. 1986 . Benthic associations and their environmental significance in the Lusitanian Basin (Upper Jurassic, Portugal) . Neues Jahrbuch fUr Geologie und Paliiontologie, Abhandlungen 172, 271 -329 . Gray, J. 1988 . Evolution of the freshwater ecosystem: the fossil record . Palaeogeography, PalaeoC/imatology, Palaeo­ ecology 62, 1 - 214. Lloyd, R.M. 1964. Variations in the oxygen and carbon isotope ratios of Florida Bay molluscs and their environmental significance . Journal of Geology 72, 84- 1 1 1 . Mook, W . G . 1971 . Paleotemperatures and chlorinities from stable carbon and oxygen isotopes in shell carbonate. Palaeogeography, PalaeoC/imatology, Palaeoecology 9, 245 - 263 .

Conclusions

4 . 1 9 . 4 Oxygen Levels from

By using a combination of facies analysis, diversity studies, and taxonomic uniformitarianism, brackish water faunas of marginal-marine environments can be recognized with some assurance . In Cenozoic and even Mesozoic rocks faunal assemblages can be assigned to specific salinity ranges (e . g . Fiirsich & Werner, 1986) . Where fossils are well preserved, isotopic analyses provide further quantification . In Palaeozoic rocks, taxonomic uniformitarianism is at best doubtful, and variations in the isotopic composition of ocean water may have occurred . We have the prospect of studying the origin and evo­ lution of the brackish and freshwater fauna that we know today, which goes back at least to the Meso­ zoic. It is uncertain whether Palaeozoic brackish water taxa (e .g. in the Carboniferous Coal Measures) are the direct ancestors of the modern taxa . We may eventually elucidate the fundamental controls on the nature and history of these successive faunas (Gray 1988) .

Biofacies and Trace Fossils

D . J . B O T TJ E R & c . E . S A V R D A

Introduction

Marine strata deposited in environments character­ ized by low levels of bottom-water oxygenation are common in the Phanerozoic stratigraphic record . These strata are important as petroleum source beds and as the common host rock for many fossil­ Lagerstatten, such as the Cambrian Burgess Shale (Section 3 . 1 1 .2) and the Jurassic Posidonienschiefer (Section 3 . 1 1 . 6) . Such strata also act as important indicators of both long- and short-term fluctuations in levels of oxygenation and, hence, circulation rate in the Earth's oceans . These factors have pro­ duced a need for continued refinement of biofacies models that permit the reconstruction of palaeo­ oxygenation of ancient basin bottom-waters .

4 . 1 9 Fossils as Environmental Indicators Early attempts to provide a framework for recon­ struction of palaeo-oxygen levels employed a uni­ formitarian approach, through analysis of faunas and sediment fabric across oxygen gradients in Recent marine basins (Byers 1977) . These studies divided such environments into aerobic (more than 1 . 0 mIlL O2), dysaerobic (0 . 1 - 1 . 0 mIlL 0 2) and anaerobic (less than 0 . 1 mIlL O2) zones (Fig. lA) . In turn, these marine zones have been used to define oxygen-related biofacies in ancient strata (Byers 1977) . Aerobic biofacies have been recognized on the basis of a thoroughly bioturbated sedimentary fabric and diverse assemblages of relatively large, heavily calcified body fossils . Dysaerobic biofacies, also characterized by bioturbated sediments, have been defined on the basis of the occurrence of low diversity assemblages of small, less heavily calcified body fossils or the absence of body fossils al­ together. Anaerobic biofacies have been delineated on the basis of the preservation of primary varve­ like lamination and the absence of in situ macroben­ thic body fossils . Anaerobic strata may, however, contain well preserved remains of nektic or epi­ planktic invertebrates and vertebrates . This oxygen-related biofacies model has been significantly refined and expanded through ad­ ditional studies of both modern environments and the stratigraphic record (Savrda & Bottjer 1986, 1987) . Major refinements include: (1) the addition of two other potentially useful biofacies, the anoxic and exaerobic biofacies; and (2) the development of a sensitive trace fossil model for reconstructing palaeo-oxygen levels within the broad dysaerobic realm. Development of the biofacies model

As originally defined, anaerobic environments may contain extremely low concentrations of dissolved oxygen . Despite the exclusion of bioturbating macrobenthic organisms, these environments may host preservable benthic microfauna, such as fora­ minifera and other soft-bodied components, that may result in microbioturbation (a subtle incom­ plete disruption of primary lamination) . In contrast, anoxic biofacies represent environments totally de­ void of oxygen. Anoxic biofacies, although they may be characterized by similar allochthonous fau­ nal elements, may be distinguished from anaerobic biofacies by the absence of in situ benthic micro­ fossils and microbioturbation (Fig. lA) . Early oxygen-related biofacies models postulated a decrease in organism size and degree of calcifi-

409

cation, as well as a drastic reduction in the relative percentage of fauna possessing calcified skeletons, as oxygen levels decrease toward the dysaerobic­ anaerobic boundary (Fig. lA) . Application of these earlier models led to the interpretation that all macroinvertebrate fossils found in laminated strata were planktic, nektic, or epiplanktic. However, more recent studies (e .g. Savrda & Bottjer 1987) of mod­ ern marine environments have demonstrated that large, well calcified macrobenthic invertebrates may occur in the lower ranges of the dysaerobic zone . In addition, subsequent studies of ancient strata suggest that some shelled epibenthic organisms may have lived on the sea floor in environments where substrates were sufficiently oxygen-deficient to exclude more active, bioturbating infauna (e . g . Savrda & Bottjer 1987) . In portions o f the Monterey Formation (Miocene, California) the bivalve Anadara montereyana occurs in situ almost exclusively in strata deposited at the dysaerobic- anaerobic boundary. Based on this occurrence, Savrda & Bottjer (1987) proposed a new oxygen-related bio­ facies, the exaerobic zone. They further postulated that these bivalves may have favoured such oxygen­ deficient environments because of a symbiotic as­ sociation with sulphur-oxidizing bacteria, although other (as yet undiscovered) processes may also be responsible for producing this phenomenon. By considering variations in basin configuration and palaeoceanographic conditions, deposition under exaerobic conditions may also explain the occur­ rence of other epibenthic faunal elements (princi­ pally bivalve molluscs and brachiopods) in laminated, unbioturbated strata that are transitional between laminated strata which lack in situ body fossils, and bioturbated dysaerobic strata, in a wide variety of Phanerozoic marine sequences . The use o f trace fossils

In the biofacies model, general sedimentary fabric plays a crucial role in determining the boundary between the anaerobic (or exaerobic) and dysaerobic zones . Recent studies have shown that discrete trace fossils can be incorporated into a model for deter­ mining palaeo-oxygen levels within the dysaerobic biofacies (e .g. Savrda & Bottjer 1 986) . The trace fossil model involves the synthesis of ichnological criteria that are based on trends in diversity, burrow diameter, and vertical extent of biogenic structures, all of which decrease with reduced oxygen avail­ ability in bottom-waters (Fig. lA) . These trends are analysed along with cross-cutting relationships of

4 Palaeoecology

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Fig. 1 A, Schematic representation of five oxygen-related biofacies described in the text. In order of decreasing levels of oxygenation, these are : (1) aerobic; (2) dysaerobic; (3) exaerobic; (4) anaerobic; and (5) anoxic biofacies . Presence and extent of the exaerobic zone depends on basin configuration and palaeoceanographic conditions (see Savrda & Bottjer 1987) . Note reduction of diversity, burrow diameter, and vertical extent of biogenic structures with decreasing oxygenation within the dysaerobic zone. B - D, Schematic illustration of trace fossil assemblages and cross-cutting relationships expected in strata deposited at various points along the dysaerobic oxygenation gradient. E, Schematic illustration of the construction of palaeo­ oxygenation curves for strata deposited in dysaerobic environments employing the trace fossil tiering model detailed by Savrda & Bottjer (1986), with permission from Macmlllan Magazines Ltd.

trace fossils, which allows the recognition of tiering relationships (Section 1 . 7. 1 ) . The model permits the delineation of oxygen-related ichnocoenosis (OR!) units, or units of strata that were deposited under similar levels of bottom-water oxygenation (Fig . lB - D) . When applied in detailed vertical sequence analyses, the trace fossil approach can be used to construct interpreted oxygenation curves that reflect rates and magnitudes of temporal change in redox conditions (Fig. lE) (see Savrda & Bottjer 1986, 1987, for examples from the Cretaceous Niobrara Formation of Colorado and the Miocene Monterey Formation of California) . Considering the prepon­ derance of the dysaerobic biofacies in the strati­ graphic record, trace fossils are thus, at our current level of understanding, the best evidence available for evaluating ancient oxygen-deficient environ-

ments . However, continued work on geochemistry and macroinvertebrate body fossils is needed to reveal additional insights into relationships between biota and oxygen levels in marine environments through the Phanerozoic.

References Byers, CW. 1977. Biofacies patterns in euxinic basins: a general model. In: H . E . Cook & P. Enos (eds) Deep-water carbonate environments, pp. 5 - 1 7 . Special Publication of the Society of Economic Paleontologists and Mineralogists No. 25. Savrda, C E & Bottjer, D.J. 1986. Trace-fossil model for recon­ struction of paleo-oxygenation in bottom waters. Geology .

14, 3 - 6. Savrda, C B . & Bottjer, D.J. 1987. The exaerobic zone, a new oxygen-deficient marine biofacies . Nature 327, 54- 56 .

4 . 1 9 Fossils as Environmental Indicators

4 . 19 . 5 Depth from Trace and Body Fossils G . E . FARROW

Depth a s such i s unlikely t o have limited a fossil organism's distribution during life . However, because many critical limiting factors are in some way related to depth, their combined effect may re­ strict the occurrence of particular organisms to a cer­ tain bathymetric range . Ecologically, the important parameters are food supply, light penetration, sub­ strate mobility, rate of sedimentation, temperature, salinity, and dissolved oxygen . Geologically, the useful parameter is depth . Indications of depth may be obtained from the overall characteristics of a fossil assemblage and its mode of preservation; from a detailed study of particular taxa, especially if they are still extant; by considering the balance of benthic and pelagic groups; or by the identification of ichnofacies . Inner versus outer shelf depths may often be inferred from the dominant fossil groups in an

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41 1

assemblage . Molluscan-dominated inner shelf as­ semblages, often with Lingula, may be contrasted with bryozoan/brachiopod-dominated outer shelf assemblages, often with ahermatypic corals or crin­ oids. Only one fossil group, however, definitively indicates shallow water - the benthic algae . Since they are dependent upon sunlight, they define the photic zone . The depth limit of the photic zone depends principally upon latitude and water tur­ bidity. Today in the clear waters of the tropics it lies at 250 m, rising to 185 m on seamounts at 47°N, and to 90 m on oceanic plateaux at 59°N. Shelf areas like the North Sea have photic limits of 22 -45 m, though this shallows to less than 1 m in estuaries . Calcareous green algae assimilate most strongly in the red part of the spectrum and are therefore restricted to shallower water than the red algae, which are adapted to · blue-green wavelengths. Rhodoliths are thus found on the shelf edge in the tropics, whereas dasyclads always indicate water only a few metres deep . Algae are noticeably absent from some carbonate facies, as for example from the basinal pioneering stages of stromatoporoid mounds in the Belgian Devonian; from Carbonifer­ ous mud mounds of the Waulsortian type (Lees et al . 1985); and from the Danian coral banks of southern Sweden, which grew in depths of 50 - 100 m. Endolithic algal borings also show bathymetric zonation. Different types characterize particular depths, and these are well preserved in shelly shelf assemblages from the Silurian of New York State and the Miocene of North Carolina, for example

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4 Palaeoecology

412 D E N S E P O P U LATI O N S FEW SPECI ES

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(Golubic et al. in Frey 1975) . Shell-boring algae may be fed upon by gastropods which leave diagnostic grazing patterns . These occur on ammonites from certain Cretaceous shales, indicating a depth of no more than 30 m for their deposition . Pelagic organisms, such as coccoliths, diatoms, radiolarians, pteropods, and graptolites, are rare in shallow water but are often abundant in outer shelf or bathyal settings . Planktic : benthic ratios provide a sensitive measure of outer shelf depths, in conjunction with maximum foraminiferal test size (Fig. 1 ) . Extrapolation o f known present-day ranges for particular taxa is perhaps the commonest empirical method of interpreting palaeodepth . Outstanding syntheses using benthic foraminifera (Natland in Ladd 1957) and molluscs (Woodring in Ladd 1957) have plotted the fluctuating Tertiary water depths in the highly active Los Angeles and Ventura strike­ slip basins . Latitude and faunal province must first be taken into account because organisms are temperature- rather than depth-dependent and classically exhibit 'tropical submergence' . The method has obvious pitfalls if the living taxon has been poorly sampled or is less common than in the fossil record, as with many ahermatypic corals (Wells in Hallam 1967) . Mapping belts of maximum faunal diversity may give useful depth indications . With microfauna this occurs just inside the shelf edge, a fact which has enabled changes in shelf gradient through the Oligocene of the Gulf of Mexico coast to be plotted (Fig. 2) . With modem macrofauna it occurs just below mean wave base, at surprisingly shallow depths, even in macrotidal shelf seas (16 m for the southern North Sea: Dorjes in Frey 1975) . This seems at variance with the situation in Silurian brachiopod­ dominated fossil assemblages, where greatest

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Fig. 4 The six universal depth-related ichnofacies of Seilacher in Hallam (1967), known from the Cambrian to the Recent: (1) Scoyenia; (2) Skolithos; (3) Glossifungites; (4) Cruziana; (5) Zoophycos; and (6) Nereites .

diversity (admittedly of preserved species only) apparently occurs nearer the shelf edge . Studying the taphonomy of a fossil assemblage may resolve such matters, since taphonomy is strongly depth-sensitive (see Section 3 . 5) . Distinct boundaries between animal communities occur at mean wave base and storm wave base (Dorjes in Frey 1975; Fig. 3 ) . Inshore of mean wave base the preservation of skeletal remains and trace fossils is controlled by hydrographic energy. Offshore, fossils are largely in situ and preservation is controlled by benthic productivity, except where interrupted by storm events . The problem of possible reworking is avoided by using trace fossils as depth indicators . Because of their long time range, depth comparisons can be made between strata of radically different age using Seilacher's universal ichnofacies concept (Fig. 4) . This has also proved of great value in broad-scale basin analysis, enabling Palaeozoic subsidence patterns in the Oslo and Central Appalachian basins to be compared (Seilacher in Hallam 1967) . The six ichnofacies do not always occur in the expected bathymetric zone (see discussion in Frey & Pemberton 1984) . Zoophycos, for example, occurs in shallower water in the Carboniferous than in the Mesozoic; and Skolithos has been recorded from proximal submarine fan facies . These anomalies occur because depth itself is not the limiting factor. Instead a combination of ecologically more signifi­ cant parameters, in this instance levels of dissolved oxygen and substrate mobility, which do not always decrease with depth, determine distribution. References Frey, R.W. (ed . ) 1975 . The study of trace fossils . Springer­ Verlag, New York.

4 . 1 9 Fossils as Environmental Indicators Frey, R. W. & Pemberton, S . G . 1984. Trace fossil facies models. In : R.G. Walker (ed . ) Facies models, 2nd edn . Geoscience Canada Reprint Series, No . 1, pp . 189 -207. Hal!am, A. (ed . ) . 1967. Depth indicators in marine sedimen­ tary environments. Marine Geology 5, 329 - 555 . Imbrie, J. & Newel!, N.D. (eds) 1964 . Approaches to paleo­ ecology. Wiley, New York.

413

Ladd, H . 5 . (ed . ) 1957. Treatise on marine ecology and palaeo­ ecology. Vol. 2: Paleoecology. Memoir of the Geological Society of America, No. 67. Lees, A., Hal!et, V. & Hibo, D . 1985. Facies variation in Waulsortian buildups, Part 1: a model from Belgium. Geological Journal 20, 133- 158. Murray, J.W. 1979 . Initial Reports of Deep Sea Drilling Project 48, 415 -430.

TAXONOMY,

5

PHYLO GENY,

A N D B I O STRATI G RAPHY

The head region, including part of the apparatus, of the first conodont animal discovered preserving soft tissues - from the Lower Carboniferous Granton Sandstones, Ingham . )

x

60 . (Photograph courtesy of J . K .

5 . 1 Rules of Nomenclature

5 . 1 . 1 International Codes of Zoological and B otanical Nomenclature

1986) . Names are admitted into zoological nomen­ clature if they satisfy the criteria of availability (Articles 10 - 20) . These are a set of objective tests that are usually easy to apply . Basically a name, to be available, must be published (in the sense of Articles 8 and 9) after 1757, accompanied by a de­ scription, and in accordance with the Principle of Binominal Nomenclature . The operation of the present Code (International Commission on Zoological Nomenclature 1985; with 88 Articles and 83 Recommendations) relies on six basic principles: Binominal Nomenclature, Priority, First Reviser, Co-ordination, Homonymy, and the Principle of Name-bearing Types .

M . E . TOLLITT

Introduction

Nomenclature is the international currency of communication among biologists . It enables any given taxon to be recognized world-wide by a unique name . An obvious premise for this is that all names must be in a single language . In both zoology and botany this was originally Latin; in zoology at least it now incorporates so many non-Latin words that it can only be called 'the language of nomencla­ ture' . The basic principle underlying both zoological and botanical nomenclature is the concept of priority as determined by the date of publication. However, the rules for determining priority in the two disci­ plines differ in important respects . These differences go back to 1842 when the British Association for the Advancement of Science set up a committee to draft a single code on biological nomenclature from which the botanists withdrew . The resulting 'Stricklandian Code' was of seminal effect in palaeozoology and neozoology but not in botany. The subsequent divergence in the historical development of the two codes since that time (see McNeill & Greuter in Ride & Younes 1986; Ride in Ride & Younes 1986) is such that each is considered separately here .

1 The Principle of Binominal Nomenclature (Article 5) demands that a species name must be a combination of two names - a binomen. For convenience the starting point for zoological nomenclature is arbi­ trarily taken to be 1 January 1758, with the two earliest wholly binominal works, the tenth edition of Linnaeus' Systema Naturae and Clerck's Aranei Svecici, deemed to have been published on that date . 2 The Principle of Priority (Article 23) simply states that the oldest available name for a taxon is its valid name . However, names established for collective groups and ichnotaxa do not compete in priority with other genus-group names . 3 The Principle of the First Reviser (Article 24) enables the precedence of one name over another to be determined when normal priority cannot be estab­ lished, as in the case of simultaneous publication. The First Reviser is essentially the first author to cite together names (or nomenclatural acts) pub­ lished on the same date, or different original spel­ lings of the same name, and to have chosen one of them over the other. Contrary to popular belief 'page priority' plays no part in determining pre­ cedence . 4 The Principle of Co-ordination (Articles 36, 43, 46) states that within the family group, genus group, or species group, a name established for a taxon at any rank in that group is deemed to have been simul­ taneously established with the same author and date as for taxa based on the same name-bearing type at other ranks in the group . The rationale for this principle lies in the subjective nature of the decision

International Code of Zoological Nomenclature

The zoological Code faces enormous problems from the sheer size of its subject matter. Well over a million species, fossil and extant, have been described and several thousand new ones are de­ scribed each year, with over a thousand new genera. The facility with which new matter can be published and the speed of development of new production technologies makes fixing the date of publication of a work ever more difficult (Ride in Ride & Y ounes

417

418

5 Taxonomy, Phylogeny, and Biostratigraphy

to allot sub- or super-taxonomic rank to a family, genus, or species . There is clearly no objective differ­ ence between taxa all based on the same name­ bearing type - thus the establishment of one implies establishment of the other or others . 5 The Principle of Homonymy (Article 52) ensures that every taxon governed by the Code (i. e . from subspecies to superfamily) has a unique name different from any other. The senior name of one or more homonyms is the valid name; the junior homonym must have its name replaced . However, in certain circumstances (Article 59) secondary homonyms produced by the transfer of species from one genus to another can be restored . 6 The Principle of Name-bearing Types (Article 61) states that each nominal taxon (i . e . a nomenclatural as opposed to a taxonomic taxon; see below) has, actually or potentially, its name-bearing type . Thus the name-bearing type of a nominal family-group taxon is a nominal genus, that of a nominal genus­ group taxon a nominal species and that of a nominal species-group taxon either a holotype, lectotype, neotype, or syntype series . By this means a zoologist distinguishes between the animal named and the mere name, thus combining nomenclatural rigour with taxonomic flexibility . The nominal taxon has been the subject of much discussion in comparing zoological with botanical nomenclature since the latter relies on the type of a name rather than the type of the organism named (see Melville in Ride & Younes 1986) .

International Code of Botanical Nomenclature The botanical Code (Voss et al. 1983; with 73 Articles and 60 Recommendations) also relies on six basic principles :

Principle I. Botanical nomenclature i s independent of zoological nomenclature . Thus, identically spelled names can exist validly under each code . The corre­ sponding rule in zoology (Article 1c) has not the status of a Principle .

Principle Il. The application of names of taxonomic groups is determined by means of nomenclatural types .

Principle Ill. The nomenclature of a taxonomic group is based upon priority of publication . This principle is concomitant with the Principle of Priority in the zoological Code and is based on the same rationale .

Principle IV. Each taxonomic group with a particular circumscription, position, and rank can bear only one correct name, the earliest that is in accordance with the Rules, except in specified cases . This Prin­ ciple is analogous with the Principle of Homonymy in the zoological Code .

Principle V. Scientific names of taxonomic groups are treated as Latin regardless of their derivation .

Principle VI. The Rules of nomenclature are retro­ active unless expressly limited .

Operational procedures in zoological nomenclature As there can be only one international code of rules for any given system of scientific nomenclature, so there can be only one body to administer it and deal with difficulties encountered by zoologists in apply­ ing it . For zoologists this is the International Com­ mission on Zoological Nomenclature, established in 1895 . The Commission' s first task was to produce a new set of rules to supersede not only the Strick­ landian Code, but also a number of other codes of limited scope that had developed in the interim . The authority of the Code depends on the willing­ ness of palaeozoologists and neozoologists to accept and use it. It can never wholly correspond to the needs of all its clients, for they have total freedom to express their taxonomic opinions as they choose . The fact that most of them seek to do so in ever more complicated ways tends to produce more complicated rules of nomenclature, and this gener­ ates a tension between those responsible for the Code (the Commission) and its users, who would naturally prefer the Code to be as simple as possible . The Commission thus has two basic responsi­ bilities : (1) it must prepare modifications to the Code to meet newly perceived requirements (leading eventually to a new edition of the Code), and (2) it must deal with problems caused by mismatches between the rules and published nomenclatural acts . Its area of operation covers all names from sub­ species to superfamily published since 1757. In this second area of responsibility the Commission has plenary powers to suspend, under prescribed con­ ditions (Article 79) the application of any provision of the Code where, in its view, such application would disturb stability or universality or cause con­ fusion . In this, and in all its actions, the Commission

419

5. 1 Rules of Nomenclature is governed by its Constitution, which is considered an integral part of the Code (Appendix F) . To achieve these responsibilities the Commission must sustain an open dialogue with palaeozo­ ologists and neozoologists everywher e . It does this by personal contact, correspondence, and through its quarterly publication, The Bulletin of Zoological Nomenclature. This contains formal applications to the Commission for the solution of particular nomenclatural problems, or for changes to the Code; comments on these applications; and the eventual decisions of the Commission . The Commission's decisions (termed Opinions) in individual cases are final (though always open to review if found to be incomplete or defective) . Its decisions (termed Declarations) on proposed amendments to the Code or Constitution are pro­ visional until they have been approve d by the body to whom the Commission reports, the Section on Zoological Nomenclature of the International Union of Biological Sciences.

that have dogged zoological nomenclature . Spread­ ing of the workload has meant that costs have been equally spread . Moreover, the broad organizational base has meant that in recent years the botanical Code has been universally accepted amongst the botanical community.

References International Commission 00 Zoological Nomenclature . 1985 . International Code of ZooltJgical Nomenclature. Adopted by the XXth General Assembly of the International Union of Biological Sciences, 3rd edn. International Trust for Zoological Nomenclature , London . Ride, W.D.L. & Younes, T. (eds) 1986. Biological nomenclature today. International Union of Biological Sciences Mono­ graph Series, No . 2 . Voss, E . G . , Burdet, H.M. , Chaloner, W . G . , Demoulin, V . , Hiepko, P . , McNeill, J . , Meikle, R.D., Nicolson, D . H . , Rollins, R . e , Silva, P. e. & Greuter, W. (eds) 1983. International Code of Botanical Nomenclature. Adopted by the Thirteenth International Botanical Congress, Sydney, August, 1981 . Bohn, Scheltema and Holkema, Utrecht; W. Junk, The Hague .

Operational procedures in botanical nomenclature In comparison with zoological nomenclature, botanical nomenclature is more highly structured in its operations, thereby giving it a broader and more secure power base . Modification of the botanical Code can only be made by the plenary session of an International Botanical Congress acting on proposals approved by the Nomenclature Section of the Congress which meets beforehand and which any botanist present at the Congress is free to attend . Nomenclatural activity between Congresses is in thE hands of a General Committee, an Editorial Committee for the Code, a number of 'Permanent Nomenclatural Committees' dealing with particular plant groups covered by the Code, and a numb er of ad hoc committees set up to report to the next Congress . The International Assodation for Plant Taxonomy (IAPT) plays a key role in botanical nomenclature with a special section of its journal, Taxon, given over to the publication of nomenclatural matters, such as proposals to conserve name s, amend the Code, etc . The final plenary session of each Botanical Congress adopts any proposals of the Nomenclature Section to amend the Code and approves the names for conservation or rejection. The decentralized organizational structure of botanical nomenclature has a number
5 . 1 . 2 Disarticulated Animal Fossils R . J . A L D RI D G E

Introduction Names in zoological rlOmenclature are given to complete animals . In p alaeontology knowledge of these animals is gained almost without exception from only incomplete re mains, most commonly bio­ mineralized skeletons . There are few problems in taxonomic treatment o:r nomenclature where the preserved fossil material forms a major part of the living animal, but diffiwlties potentially arise when the skeleton comprise d multiple components of differing morphology that became disarticulated and scattered on the dea.th of the animal and decay of the soft tissue . Thes;e components may not be recognized as belonging to the same animal, or there may be uncertaint�es or differences of opinion regarding the complete skeletal composition. Some authors have consequently advocated a system of para taxonomy to a.ccommodate fragmentary remains . A para taxon WillS defined by Melville (1979, p. 14) as 'a taxon based on a fragment or detached

420

5 Taxonomy, Phylogeny, and Biostratigraphy

organ of an animal which can be classified at genus ­ group and species- group levels by comparison with other fragments or detached organs, but cannot be assigned to the same taxa at those levels as the whole animal to which they belong' . In practice, parataxonomy is outside the orthotaxonomy of the same group of organisms, being based on a particu­ lar, fragmentary, sort of material (Bengtson 1985) . The success of workers on fragmentary remains, particularly specialists in conodonts, in pursuing the taxonomy of their groups without recourse to parataxonomy, has resulted in the latter not being admitted to the International Code of Zoological Nomenclature (Section 5 . 1 . 1) . Under Article 23(f) (i) of the Code, the Principle of Priority is held to apply 'even if any part of an animal is named before the whole animal' . The procedures adopted in the nomenclature of fragmentary fossils and of the par­ tially or completely known skeletons of which they were components can be illustrated by reference to current practice in conodont taxonomy. Conodonts and parataxonomy

Conodonts were soft-bodied marine animals which possessed a feeding apparatus constructed from microscopic phosphatic elements; their strati­ graphical range is Upper Cambrian - uppermost Triassic. The fossil record of the group consists almost entirely of disjunct elements, which are normally recovered through mechanical or chemical disaggregation of rock samples . Collections made in this way may contain elements from several differ­ ent coexistent species . Rarely, complete or partial apparatuses of individual animals are found pre­ served intact on bedding planes (Fig . 1) or as fused clusters in acid-insoluble residues, giving direct evidence of the apparatus composition of some species . The apparatuses of many other species have been partly or completely reconstructed using morphological and distributional criteria, and most conform to a limited number of structural plans . Until the mid nineteen-sixties each morphologi­ cally distinct element type was given its own bino­ men, following an initial belief by some specialists that every animal contained elements of only one type. However, specimens of complete apparatuses on bedding planes, first discovered in 1 934, prove that each individual contained several components of up to eight different types . A dual nomenclature developed, with separate names for completely pre­ served apparatuses existing alongside the names for the element types . This procedure is outside the

1 Complete apparatus of a single conodont animal preserved on a bedding plane; specimen x-6377, University of Illinois, from the Carboniferous of Illinois ( x 32) . Fig.

Code and becomes unworkable in practice when applied to partially known apparatuses or to those reconstructed through studies of isolated elements . At an international symposium held in 1971, conodont specialists agreed to dispense with dual nomenclature and to follow the Principle of Priority in naming multielement, apparatus-based taxa. Nomenclature of apparatus-based taxa follows two steps : consideration of the valid specific name and consideration of the appropriate generic name (Fig. 2) . For many apparatus-based taxa, some or all of the component elements may already bear separ­ ate names . The valid specific name for the apparatus­ based taxon is the oldest of these names, provided that the holotype bearing that name can be demon­ strated to belong or probably belong to the apparatus-based species under consideration . This can usually be assessed by the examination of other elements found in association with the holotype . In cases where the oldest name was allocated to a characteristic element of the apparatus, no difficult­ ies arise . Where the oldest species name is borne by a specimen representing an element of conservative morphology, repeated in many species, then the nature of the other elements associated with the

421

5 . 1 Rules of Nomenclature

E Fig. 2 Element types in the reconstructed Silurian conodont apparatus of Ozarkodina confluens (Branson & Meh1 1933) x 33. Originally, Branson & Mehl gave each element type a separate name : A, Spathodus primus; B, Ozarkodina typica; C, Trichognathus symmetrica; D, Prioniodus bicurvatus; E, Hindeo­ della confluens; F, Plectospathodus flexuosus. As all six species names were published in the same paper, their relative precedence was determined by Jeppsson (1969), who as First Reviser (see Section 5 . 1 . 1 ) chose the name confluens; the other five are subjective junior synonyms . The appropriate generic assignment is not to Prioniodus, the oldest name, nor to Hindeodella, the next oldest. The Ordovician type species of Prioniodus has a different apparatus from that of confluens, while the apparatus of the Devonian type species of Hindeo­ della is unknown. Spathodus and Trichognathus are junior homonyms of older names and were not replaced until after 1933 . Ozarkodina and Plectospathodus were both erected in 1933, with O. typica and P. flexuosus as their type species, and either might be used as the generic name; Ozarkodina was selected by Lindstrom (1970) .

holotype is crucial. If these are unknown and cannot practicably be determined by re-collecting the type horizon, then the oldest name is treated as a nomen dubium and the next oldest available name comes under consideration. The procedure for allocating an appropriate gen­ eric name is similar. In this case, the oldest generic name borne by any element included in the appar­ atus is selected, provided that the type species of that genus can be demonstrated to be congeneric or probably congeneric with the apparatus-based taxon under consideration . If the type species is not congeneric or is based on an element from an un­ known apparatus, then the next oldest available name is considered. Exceptions to this procedure occur when the apparatus-based taxon can be shown

to belong to an established apparatus-based genus with an older name . If none of the elements provides an appropriate generic name, and there is no prior name available from congeneric species, a new name is required . Stability of nomenclature is achieved through the determination of the apparatus structures of the holotypes of each species and of the type species of each genus . Until this is attained for all existing names, a few that have been treated as nomina dubia may become available as knowledge about their apparatuses is acquired, and they may prove to be senior synonyms of names currently in use . In the absence of unequivocal knowledge of all appar­ atuses, there will always be some taxa that are known or believed to represent only part of the skeleton, other parts of which may carry different names . For these, Bengtson (1985, p. 1354) intro­ duced the term sciotaxon, defined as a 'taxon that is considered to represent the same real taxon as another taxon based on material of a different nature' . This concept has application in all groups where fossil representatives are commonly fragmental. References Bengtson, S . 1985 . Taxonomy of disarticulated fossils. Journal of Paleontology 59, 1350 - 1358 . Branson, E.B. & Mehl, M . C . 1933. Conodont studies, no . 1 . The University of Missouri Studies 8 , 1 - 72, 4 pIs . Jeppsson, L. 1969 . Notes on some Upper Silurian multi­ element conodonts . Geologiska Fiireningens i Stockholm Fiirhandlingar 91, 12-24. Lindstrom, M. 1970 . A suprageneric taxonomy of the cono­ donts . Lethaia 3, 427-445 . Melville, R.V. 1979 . Further proposed amendments to the International Code of Zoological Nomenclature Z . N . (C . ) 182. Bulletin of Zoological Nomenclature 36, 1 1 - 14.

5 . 1 . 3 Disarticulated Plant Fossils B . A . THOMAS

Introduction

Whole plants are only very rarely preserved in the fossil record . The vast majority of plant fossils are organs, or pieces of organs, that were shed in life,

422

5 Taxonomy, Phylogeny, and Biostratigraphy

broken off, or detached after death . There have been several successful reconstructions of whole plants but these are exceptions rather than the rule . Therefore, the major problem confronting anyone studying plant fossils is how to name and classify these very different fragments . Naming is in essence identifying and it constitutes what is called no­ menclature . Principle IV in the International Code of Botanical Nomenclature states 'Each taxonomic group with a particular circumscription, position, and rank can only bear one correct name, the earliest that is in accordance with the Rules, except in specified cases' (see also Section 5 . 1 . 1) . Such a principle is much more difficult to follow with fossils than with living plants for observations are limited almost exclusively to morphological and anatomical characters . Palaeobotanists use a system of nomenclature for isolated organs, whereby the leaves, stems, roots, and various parts of reproductive organs receive different generic and specific names. Such a system enables information to be assembled not only for species lists but for evolutionary, ecological, and stratigraphic purposes. Even so, there are many problems which may be approached in various ways . Papers in Spicer & Thomas (1986) summarize the interrelated problems and the methods of using the available information. Organ genus and form genus

Much debate has centred on the concept of the genus as applied to plant fossils and on the use of the organ genus and form genus (see Chaloner in Spicer & Thomas 1986 for discussion) . Organ genera are based on fossil organs that can be assigned to families and higher taxa. Form genera are based on less well understood fossils that cannot be assigned to families . Any fossils that are completely known as whole plants can be assigned to genera as if they were living plants . Based on this conception, the use of nomenclatural priority should ensure a work­ able system, and generic keys may then be con­ structed for identification purposes (e .g. Thomas & Meyen 1984) . Modern names for plant fossils

There is a case for using modem names for some plant fossils when their diagnostic suites of charac­ ters fall within a characteristic range of variation of comparable organs of living genera or species, e . g . Gingko, Metasequoia, and many o f the Tertiary

genera of leaves and seeds (Collinson in Spicer & Thomas 1986) . However, the use of a modem bi­ nomen for a fossilized organ must not be taken to imply that the whole plant had the same botanical characteristics as the living genus or species . Un­ substantiated extrapolations via whole plants to their past phylogeny, ecology, and environmental parameters might be completely incorrect. Organic connection between taxa

Sometimes organs that have received different gen­ eric names are found in organic connection, e . g . the Carboniferous lycophyte cone with Lepidostrobo­ phyllum megasporophylls has been found attached to leafy shoots assignable to Lepidophloios and mega­ spores Cystosporites recovered from the cones . By such means whole plants may be reconstructed (Fig. 1) . Occasionally two genera may be shown to repre­ sent parts of the same plant, even though they are preserved in different ways, e . g . petrified fragments of the stem of the compression Archaeopteris have the same anatomy as the wood Callixylon . This gave Beck (1960) the concept of the Progymnosperms . Even though it may seem unnecessary to retain the various generic names, it is best to do so . Even if an organic connection between some species is known, there is no certainty that all species of these genera will be shown to have been connected in this way . Indeed, as organs are likely to have evolved independently, there is every reason for keeping both names, especially if they might well have different stratigraphic ranges . Evolution and change

Early evolutionary radiation of any group will pro­ duce organisms that share a mixture of morphologi­ cal characters . Only later will they be sufficiently distinct to be recognized as taxa. Spicer and Burnham (independently in Spicer & Thomas 1986) have suggested methods of using systems of group­ ing specimens into morphological forms, thereby having an alternative, but parallel, scheme to the generally used Linnaean system. Hughes (e .g. in Spicer & Thomas 1986) has similarly suggested an alternative data handling scheme for early angiosperm-like pollen. Classification

The use of the binominal system of nomenclature

423

5. 1 Rules of Nomenclature

Cystosporites L epidocarpon

Whole plants are rarely fossilized intact, so reconstructions, such as this Carboniferous arbor­ escent lycophyte, are based on evidence from detached plant parts, each of which usually has its own name . Knorria is the name given to old wrinkled bark, and Lepidophloios one name given to fossils of leaf­ cushion covered stem. Leaves are referred to as Lepidophylloides and the rhizophore rooting system as Stigmaria. Microsporangiate cones (Lepidostrobus) yield Lycospora microspores. The megasporangiate cone has Lepidostrobophyllum sporophylls with one functional megaspore (Cystosporites) per sporangium. Comparable permineralized megasporangiate sporophylls are called Lepidocarpon . (From Thomas & Spicer 1987.)

Fig. 1

/

Lepldophyl/oides

L epidostrobus [I 1\ 1

Lepidophloios

,I

Lycospora

I.

Knorria

for dispersed plant organs reflects a comparison of their morphologies . This has been extended above the generic level to classify plant fossil organs into families, orders, and subdivisions, with each clas­ sification depending on the views of the author. Many plant organs do not fit into such families and are put into an incertae sedis 'unknown' category. Another approach is to use satellite taxa, which suggest affinity to those genera in a family or order (Thomas & Brack-Hanes 1984) .

Stigmaria

Thomas, B.A. & Meyen, S.V. 1984. A system of form-genera for the Upper Palaeozoic lepidophyte stems represented by compression-impression material. Review of Palaeobot­ any and Palynology 41, 273- 28l . Thomas, B.A. & Spicer R.A. 1987. The evolution and palaeobio­ logy of land plants. Croom Helm, London .

5 . 1 . 4 Trace Fossils S . R . A . KELLY

References Beck, C . B . 1960. The identity of Archaeopteris and Callixylon . Brittonia 12, 351 - 368. Spicer, R.A. & Thomas, B. A. (eds) 1986. Systematic and taxo­ nomic approaches in palaeobotany. Systematics Association, Special Volume 31 . Clarendon Press, Oxford . Thomas, B . A. & Brack-Hanes, S . D . 1984. A new approach to family groupings in the lycophytes. Taxon 33, 247-255 .

Introduction

The status of trace fossil names has had a complex history (Basan 1979) . The 1985 International Code of Zoological Nomenclature (Section 5 . 1 . 1 ) marks an

424

5 Taxonomy, Phylogeny, and Biostratigraphy

important step in the official recognition of the need for a code of ichnological nomenclature, by taking under its wing some aspects of the problems of ichnology . Many difficulties were clearly antici­ pated by Bromley & Fursich (1980), however, and any user of the Code should be aware of the main two : 1 Trace fossils may b e made b y the activity o f any organism, whether animal, plant, or protist. The restriction of trace fossils to animals in the Code is an unnecessary limit to ichnology, and future use must indicate that trace fossils were not just produced by animals . 2 Traces of extant organisms can appear identical to those produced by fossil predecessors . There is no logical need to isolate Recent from fossil traces . Recent traces are incipient potential trace fossils; some, like borings and abrasions on hardgrounds, are already lithified. Whilst it is useful to have some reference to trace fossils in formal biological codes of nomenclature, these are probably not the best places for the in­ clusion of a 'Code of Ichnological Nomenclature' which is itself non-biological yet involves all bio­ logical kingdoms . There is a strong argument for the establishment of an independent ichnological code (Sarjeant & Kennedy 1973; Basan 1979), to be administered by an international body and run principally by palaeontologists (whose interest it would mainly serve) . Whilst this is an ideal aim for the future, the present article attempts to provide guidelines for the ichnotaxonomist today . Principles of ichnology

Most of the background to ichnology has been described by Ekdale et al. (1984) . Bromley & Fursich (1980) outlined six principles fundamental to trace fossil nomenclature : 1 Trace fossils are structures produced in sediments and hard substrates (either organic or inorganic in origin) by the activity of organisms (animals, plants, and protistans) . 2 The nomenclature of trace fossils is based solely upon the morphological characteristics of the structure . 3 A particular structure may be produced by the work of two or several different organisms living together, or in succession, within the structure . 4 The same individual or species of organism may produce different structures corresponding to differ­ ent behaviour patterns .

5 The same individual or species of organism may produce different structures corresponding to iden­ tical behaviour but in different substrates, e . g . in sand, in clay, or at sand - clay interfaces . 6 Identical structures may be produced by the activity of systematically different trace-making organisms, where behaviour is similar.

Establishing an ichnological name

Two codes should be consulted when establishing or revising ichnological names. The names, author­ ship, and dates of most trace fossils are covered by the 1985 zoological Code (Section '5 . 1 . 1) . Other examples may be dealt with using the proposed ichnological code of Sarjeant & Kennedy (1973) . Formal trace fossil names are form taxa and comprise an ichnogenus, ichnospecies (both ital­ icized), and author with date (placed in brackets when the name has been altered subsequent to its original establishment), e . g. Rusichnites grenvillensis (Dawson, 1864); Cruziana grenvillensis (Dawson, 1864) . The names should be treated in a similar way to Linnaean binominal zoological names. A suitable idiomorphic (i. e . showing full, uninhibited mor­ phological development) holotype should be desig­ nated, figured, and placed in a suitable institutional collection (Section 6.3.1). A name proposed for an ichnotaxon does not compete in priority with one established for an organism, even for one that may have formed the ichnotaxon. The principle of homonymy applies to all levels of ichnotaxa . The 1985 zoological Code regarded the type species as unnecessary with regard to trace fossils, although arguably such a concept is useful to provide a reference species when creating others . Supraichnogeneric nomenclature

The 1985 zoological Code indicated that only family­ level names should be used for trace fossils at formal supraichnogeneric level . In practice, higher level groupings of trace fossils are almost always informal . Hantzschel (1975) used only the following divisions : Trace Fossils, Borings, Coprolites, and Trace Fossils or Medusae Incertae Sedis . Ekdale et al. (1984) out­ lined various classifications applied to trace fossils . Bio- and ichnotaxonomic classifications are com­ monly confused, but should always be kept separ­ ate . Typical higher classifications include : 1 Biotaxonomic class ification . Whilst it is possible to identify with accuracy the constructor of some trace

5.2 Analysis of Taxonomy and Phylogeny fossils or traces in the absence of the body con­ cerned, in many cases this is highly speculative (see Principles 3 - 6 above) . Subjective . 2 Preservational classification . The relationship be­ tween the trace and its position in or on the sedi­ ment. Full relief (exichnia/endichnia), epirelief (epichnia), hyporelief (endichnia) . Objective . 3 Biological behavioural classification . Resting, crawl­ ing, grazing, feeding, dwelling, escape, coprolitic, faecal, pseudofaecal, excavation, regurgitation, plant penetration structures; even stromatolitic structures are included by some workers . Subjective . 4 Palaeoenvironmental classification . Ichnofacies dis­ tributions with relation to depth, energy, salinity; soft versus hard substrate traces . Undesirable names and constructor- trace relationships

In creating new names, palaeontologists should en­ sure that the selected name does not infer a particu­ lar architect, constructor, or tracemaker. However, existing names, such as Teredolites, which are undesirable because they imply erroneously a particular occupant or creator (in this example, Teredo), are nevertheless valid names and should be retained for the purposes of nomenclatural stability. Great care is needed by the palaeontologist to separate the concepts of trace fossils and their sup­ posed creators . Ichnotaxa should be treated as non­ biological form names only and their association with named organisms should be a matter of careful

425

discussion, especially when there is no body fossil present. Even if there is a body fossil present, it may not be that of the original constructor. Exclusions

Trace fossil names should not be applied to such fossil evidence as internal or external moulds or impressions, casts or replacements, prod and bounce marks of shells or organisms acting as trans­ ported clasts and not propelling themselves. Such structures do not represent biological activity . References Basan, P.B. 1979. Trace fossil nomenclature: the developing picture . Palaeogeography, Palaeoclimatology, Palaeoecology 28, 143- 167. Bromley, R.G. & Fiirsich, F.T. 1980 . Comments on the pro­ posed amendments to the International Code of Zoological Nomenclature regarding ichnotaxa. Bulletin of Zoological Nomenclature 37, 6 - 1 0 . Ekdale, A . A . , Bromley, R.G. & Pemberton, S . G . 1984. Ichnology, the use of trace fossils in sedimentology and strati­ graphy. Society of Economic Paleontologists and Mineral­ ogists, Tulsa, Ok . Hantzschel, W. 1975. Trace fossils and problematica. In: C . Teichert (ed .) Treatise o n invertebrate paleontology. Part W. Miscellanea, Supplement 1 , 2nd edn . Geological Society of America, Boulder, Co. , and University of Kansas Press, Lawrence, Ka. Sarjeant, W.A.S. & Kennedy, W.J. 1973. Proposal of a code for the nomenclature of trace fossils. Canadian Journal of Earth Sciences 10, 460-475 .

5.2 Analysis of Taxonomy and Phylogeny

5 . 2 . 1 Overview R . A . F O RT E Y

Taxonomy i s the science o f classification o f organ­ isms . This involves both the naming of taxonomic units, including rather dry nomenclatural aspects

which are as much legal as scientific, and the analy­ sis of morphological characters forming the basis of that nomenclature, which can be one of the most important foundations from which larger inferences are made . On the assumption that evolution has occurred, taxonomy has been much intertwined with phylogenetics, concerned with the description of evolutionary relationships . Because fossils have been assumed to be the proof (or at least the

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exemplars) of evolution, the interplay between taxo­ nomy and phylogeny has perhaps been more inti­ mate in palaeontology than in the taxonomy of living organisms . This has led to problems which are not trivial ones just to do with names. Some of these problems are discussed in this section . The rules governing the naming of organisms are not considered in detail, although they do have impor­ tance in attempting to ensure nomenclatorial stab­ ility and uniform usage throughout the scientific community (Section 5 . 1 ) .

Taxonomic basis o f palaeontological theories

Good taxonomy is the basis on which practically all other palaeontological generalizations rely; bad taxonomy will result in ill-founded and misleading theories . This can sometimes be a problem because the theorists are usually not the same people as the taxonomists . The former may even regard taxono­ mists as a bit of a nuisance and as 'nit pickers' (some are!), while taxonomists may regard their generalizing colleagues as taking unjustified lib­ erties with poor data. None the less, taxonomy and most palaeontological generalizations are inex­ tricably linked : 1 Palaeogeographic theories based on fossil taxa

always rely upon maps, or clusters of similar taxa. The analysis of patterns will only be as good as the taxonomy of the organisms included in the data. For example, palaeogeographic maps are often reconstructed from the distribution of genera, but if these genera are unnatural groupings of species, any conclusions drawn from the maps are bound to be ambiguous . 2 Synecological generalizations from the fossil record, whether concerned with the history of 'communities' through time (Section 4 . 1 7), or attempts to construct whole biota from Lagerstiitten (Section 3 . 1 1 ), rely on correct taxonomic assessment of their components . The famous Middle Cambrian Burgess Shale fauna from western Canada (Section 3 . 1 1 . 2) has been reworked from the taxonomic stand­ point in the last two decades. This has revealed important features at the community level which were not apparent from the original descriptions by C . D . Walcott, e . g . the prominence and diversity of worms of the Phylum Priapulida when compared with the Recent. 3 Analysis of patterns of diversification (Section 2 . 7) and extinction (Sections 2 . 1 2 & 13) is considered one of the ways in which the fossil record contri-

butes uniquely to biological history. The reality of such patterns depends critically on the taxonomic underpinning. Some supposed evolutionary 'bursts' correspond well with the activities of particularly diligent monographers . Recently Patters on & Smith (1987) have shown how much of the data for sup­ posed 26 million year extinction cycles of families (Section 2 . 12.3) are inadequate in one way or another - notably by including examples of 'taxo­ nomic pseudoextinction' (Briggs et al. 1987) where an apparent extinction is only the product of taxo­ nomic practice . It should not be claimed - as some extreme sceptics might - that there are no patterns of extinction or radiation in the fossil record. There surely are . The important point is that taxonomy is crucial to discriminating those patterns correctly. Why fossils pose particular problems for the taxonomist

Fossils do not always fit comfortably into classifi­ cations based on the living fauna and flora (Cracraft & Eldredge 1979) . Linnaean taxonomic categories are applied to both fossils and their living relatives, and occasional suggestions that they be replaced by something else for fossils have not found favour. The problems posed by fossils stem both from the nature of the material itself and from the introduc­ tion of the time dimension into taxonomy. The information obtainable from fossils is limited, whereas, in principle, that from living organisms is inexhaustible . Many fossils are fragmentary, nearly all lack traces of the soft anatomy, they may be distorted, and so on. Classifications of living organ­ isms are now influenced by biochemical studies, immunology, DNA analysis - and at the other end of the scale by behavioural information - virtually all of which is not available from fossil material. Modern taxonomic studies often compare relation­ ships deduced from the molecular level with cladograms based on 'classical' whole-organism morphology; where agreement between the two is good, the relationships are likely to be well founded. With fossils such independent testing is not avail­ able . Soft anatomy can, of course, be inferred from hard parts, but this may be a difficult procedure when the fossil group in question is entirely extinct. Although such preservational limitations are obvious, the influence of the temporal dimension is subtler . If there were no fossil record, the Recent fauna and flora would consist of discrete species­ level taxonomic units, each of which could be characterized genetically, and analysed by cladistic

5 . 2 Analysis of Taxonomy and Phylogeny methods into a hierarchy of relationships with the rest. The historical component - including the phylogenetic steps leading to the Recent taxa would be inferred directly from the cladograms . The existence of the fossil record means that there is direct evidence for the timing of branching events . Some zoologists use the fossil record only with this intent; for such scientists the importance of Archaeopteryx is not as an 'intermediate' between birds and Reptilia (itself a paraphyletic group), but as a chronometer dating the earliest record of some derived characters shared by all birds, e . g . feathers . This viewpoint is shared by many cladists (Section 5 . 2 . 2) . Such workers tend to place the fossils in the appropriate position on their cladograms but eschew according the extinct forms the formal (often high-level) taxonomic recognition they have received in the past. It is not surprising that fossil forms often show combinations of primitive characters in relation to their living relatives . Despite the claims of some creationists, the distribution of characters in the fossil record overwhelmingly supports the notion of descent with modification . It is this very property which has created further problems for the taxo­ nomist. In past years, palaeontologists have noted the general similarity of fossils living at the same geological time period - and such groups have been dubbed with names, which have now become familiar in the literature (the so-called mammal-like reptiles would be an example) . In this case the notion of time has become linked directly with the taxonomy. The problem is that the nature of the 'similarity' was not analysed by the original taxonomists - it merely seemed appropriate that primitive and ancient forms 'belonged together' . Much of the argument about taxonomy and fossils over the last few years is essentially about the question of what to do with such groups, which are based on shared primitive characters - and often have a similar stratigraphic age as well . From the phylogenetic point of view, units of classification (orders, families, genera, etc . ) can be one of three things : monophyletic, descended from a single common ancestor, and including all its descendants; polyphyletic, an artificial group descended from more than one ancestor (usually classified together because of a striking but super­ ficial similarity); or paraphyletic, descended from a common ancestor, but not including all descend­ ants . This last named category is the one that causes the trouble in palaeontological classifications, be­ cause it includes the units based on primitive

427

similarity - the limbs, as it were, of the evolutionary tree, without the branches and twigs . Few people today would seriously defend a classification that includes polyphyletic taxa - the story of taxonomic progress is often the story of the dismantling of polyphyletic taxa, like the old phylum which in­ cluded all the superficially worm-like animals . Cladists attempt to reduce units o f classification to monophyletic groups (Wiley 1981); other system­ atists continue to recognize paraphyletic taxa, sometimes with the reservation that it is in lieu of anything better. Cladistic analysis does not formally recognize ancestors, and the particular problem of reconciling the fossil record with such analyses is that palaeontologists, and especially invertebrate palaeontologists, recognize ancestors with some frequency.

Direct phylogenetic information from the fossil record Palaeontologists frequently describe lineages con­ necting two or more fossil taxa, which are supposed to represent hypotheses about their evolutionary relationships . Invertebrate palaeontologists, in particular, often have a prolific fossil record, with thousands of specimens from a formation or area on which to base such lineages, which are usually represented as some kind of evolutionary tree. Ancestral species are often included in such trees . Discussion of many of the macroevolutionary phenomena that form the subject of chapters in this book depends on the acceptance of the reality of these trees. Invertebrate groups yield trees that can be tested against future occurrences of species, and as such are properly scientific constructs . Foramini­ feral phylogenies, for example, are tested every time a new borehole is put down. The detailed way in which such trees are constructed varies from worker to worker, but usually involves a strati­ graphic sequence of samples (the stratophenetic method; Section 5 . 2 .4), from which species are rec­ ognized . The species are then arranged in phyletic sequence, which may or may not involve branching events where an ancestral species splits into two descendants . Gradualistic change is slow and con­ tinuous, punctuational change is rapid (often ap­ parently instantaneous as seen in the rocks); both probably occur in the fossil record, with the latter predominating. In gradualistic lineages there are problems about the arbitrariness of applying names to segments of a spectrum, but such niceties probably do not deserve the attention they have

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5 Taxonomy, Phylogeny, and Biostratigraphy

received . Punctuationally derived species are usually clearly defined entities, which should be morphologically capable of diagnosis and limited stratigraphically. Examples of such trees can be found in the literature of ammonites, graptolites, trilobites, brachiopods, and microfossils in general, but rarely in vertebrates other than mammals . These species - species lineages almost invariably involve rather small changes in skeletal morphology. Another kind of 'evolutionary' tree is to be found in the palaeontological literature . This kind is much less precise than the ones just described, often relates to higher-level taxa than species (genera, families or even higher taxa), and has been a more characteristic product of vertebrate workers . The fossil record of vertebrates is sporadic and ca­ pricious . Most records of higher taxa are separated by stratigraphic and morphological gaps, and there is little chance of reading evolutionary history directly from sequence . However, trees have been constructed from the succession of forms purporting to record 'advancement' of morphology through time; early forms have been described as ancestors in such phylogenies . This kind of loose treatment is worth distinguishing from stratigraphic species lineages, because the chances of finding an entirely appropriate ancestor in this kind of sequence are small . 'Ancestor' in this sense is used as a kind of shorthand for 'early representative retaining many primitive features' ; it is this usage which has been strenuously criticized by cladists, and with some justice . One has only to look at the recent history of the discoveries relating to the evolution of Homo and its relatives to see how each early discovery is claimed as some kind of 'ancestor', but at the same time how each major discovery has contributed to turning a simple, straight-line ape - man transition into a more complex, branched tree . Many (perhaps most) palaeontologists continue to use their phylogenetic trees as a basis for tax­ onomy . Some of these palaeontologists strive also to make their higher taxa monophyletic. But of course the recognition of ancestors poses a set of problems for which there is no formal solution. If a fossil species lies at the 'origin' of two monophyletic genera, to which is it assigned, or is it not assigned to either? It may not be clear which are primitive and which are derived characters, because fossil species are often discriminated on tiny features without a priori polarity. If a cluster of such species is otherwise united by shared, primitive (symplesio­ morphic) features, to recognize that group as a genus inevitably results in a paraphyletic grouping .

In short, the better and more complete the fossil record is (i. e . the more fully the evolutionary history is spelled out in the rocks), the more problematic becomes the strict application of cladistic classifi­ cation 'rules' . This paradox is important in under­ standing the controversy between cladists and stratopheneticists which has burgeoned in the last few years . Cladistics, stratigraphy and the reconstruction of phylogenetic history

The impact of cladistics on systematics has been profound and beneficial . Cladistics has provided a rational basis for classification which can encompass both the animal and plant kingdoms, based on objective assessment of character distributions . This has done much to dispel the subjective and often authoritarian approach to systematics that has per­ tained in the past - where the recognition of a genus, for example, depended on whether the expert happened to have felt that a species 'deserved' generic status . This is not the place to elaborate the mechanics of cladistic classification, which is treated below (Section 5 . 2 .2) . Cladistics was developed in­ itially by neontologists and enthusiastically adopted by vertebrate palaeontologists at an early stage . As stated above, it is the vertebrate fossil record which is in general subject to the largest (morphological, stratigraphic) 'gaps' and the woolliest trees, and cladistic analysis of relationships provided both a new objectivity, and a new sophistication of compu ter-based techniques . Hennig, the originator o f cladistic analysis, was clear that his intent was historical: the branches on the cladograms represented real, historical specia­ tion events (Hennig 1966) . The cladogram was, in a sense, a model of evolutionary history. For the insects with which Hennig worked there was but little fossil record, and a careful working of living taxa was the most productive approach to phylo­ genetics . Darwinian evolution is a theory - a con­ ceptual framework in which biological thinking operates. A further development of cladistics (,pattern' or 'transformed' cladistics) was to remove this theory-laden presumption from the procedure: classification should be based entirely on the pattern of distribution of characters in the cladogram, with­ out regard to any presumed evolutionary history. This attempt at objectivity has been misrepresented by certain creationists as 'scientists do not believe in evolution' , whereas the point was to make any system of belief irrelevant to the objectivity of the

5.2 Analysis of Taxonomy and Phylogeny character analysis . But what place could fossils have in this new objectivity? Fossils are, at the least, fragments of history; can they have any place in a classification system which attempts to minimize the historical component from its construction? The present status of these questions depends very much on the philosophical stance of the investi­ gator. In the first place there is no doubting the power and breadth of cladistic techniques in tax­ onomy across all classes of organisms; there is no other method of such universal applicability . It is perhaps not surprising that those who developed the methods of analysis should defend them with the fervour of those defending the true faith, and castigate dissenters forthrightly . There have been equally strong disagreements within this coterie about which analytical technique is likely to yield the most robust results . None the less it is clear that there are several possible attitudes to the fossil record even among people who would call them­ selves cladists, valuing as they do the technique of analysis for its explicitness, objectivity with regard to characters, and ready testability from new data. In an attempt to be fair to the diversity of opinion on present attitudes to taxonomy and the fossil record I have tried to summarize the differing philo­ sophical positions into a few categories . 1 Pattern cladists . Such workers contend that fossils have contributed very little to theories of relation­ ship based on Recent organisms (Patterson 1981) . The contribution of fossils lies in determining the antiquity of groups, but seldom if ever in discrimi­ nation of relationships, which fossils have in the past often confused more than clarified . These workers allow fossils their palaeobiogeographical importance, and, on occasion and in lieu of anything better, admit palaeontological evidence in the deter­ mination of character polarity . The historical, narrative contribution that fossils may make, based on sequence, is effectively eliminated. 2 Evolutionary cladists . Under this category come workers who use essentially the same cladistic methods to analyse relationships as the pattern cladists, but regard the fossil record as of importance in testing those relationships (Hill & Camus 1986) . They would regard congruence between the se­ quence of branching nodes on the cladogram and the stratigraphic appearance of the appropriate taxon in the fossil record as an important part of the scientific method, and to this extent directly acknowledge the temporal dimension that fossils offer. In the examples worked, which have only a moderate fossil record, there is a surprisingly good

429

match between the sequence on cladogram and sequence in rock . 3 Phylogenetic historians . This category of worker regards the reason for analysing character distri­ bution as the reconstruction of the phylogenetic history of the organisms analysed . Such workers regard genealogy as a fact - and, as such, capable of being reconstructed . They distinguish between the fact of genealogy and the theory of evolutionary mechanism (including Darwinism, Neutral theory and the like); the latter is testable from trees, but should in no sense be incorporated a priori in their construction . These workers admit both cladistic and strati graphic analysis into the methodology of phylogeny construction (Fortey & Jefferies 1982) according to circumstances . Both methods are re­ garded as models of phylogenetic history . For fossil groups with good, stratigraphically controlled fossil records, a stratophenetic approach is appropriate; for groups with a poor fossil record cladistic methods give results which more closely approach the reconstruction of historic branching events .

4 Stratigraphic palaeontologists and stratopheneticists . Such workers rely heavily on stratigraphic sequence to deduce phylogenetic relationships, which are drawn out as 'trees' . Ancestral species, and paraphyletic taxa are not uncommon in classifi­ cations drawn from such trees . These palaeon­ tologists often allow stratigraphy to be the arbiter of primitive and derived character states. Many (but certainly not all) workers with this approach tend to operate at the species - species level on their trees . Genera tend to become 'branches' of the trees, but in some cases (in the foraminiferal lineage Globigerinoides to Orbulina, for example; see Banner & Lowry in Cope & Skelton 1985) different generic names are applied to different steps in a single lineage : this probably represents the perfect antith­ esis to the cladistic approach to classification . It should be added that there are many more palaeontologists who conform to none of these categories, but continue to operate with rather vague notions of 'affinity' . However, any of the four attitudes listed above represents a valid scientific approach, even though the champions of one method or another might deny it! It is noticeable that the attitude to phylogeny does seem to relate to the kind of scientific problem which is under examination . Pattern cladists tend to be those who study groups with a sporadic fossil record (fishes, spiders), and whose intention is to clarify relation­ ships of living organisms, while at the other ex-

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5 Taxonomy, Phylogeny, and Biostratigraphy

treme the stratigraphic palaeontologists tend to be those who study groups with arguably complete fossil records (ammonites, foraminifera, graptolites, bivalves), and whose main concern is the correlation of rocks . At the moment there is little acknowledge­ ment of the role of either extreme by the other, and hence taxonomy is polarized . On the one hand, cladists are making new sense of classification especially at high level - and focusing attention upon characters rather than subjective notions in the definition of groups . They are also minimizing the contribution of fossils and simply do not 'see' ancestors . On the other hand, stratigraphic palaeontologists continue to describe trees at low taxonomic level - and include what they regard as proven ancestors - but fail to recognize the contri­ bution that a cladistic analysis might make to the logical ordering of their higher level classifications . Whether a compromise can b e struck, perhaps approximating to one of the historical approaches, remains to be seen .

References Briggs, D . E . C . , Fortey, R.A. & Clarkson, E . N . K . 1987. Extinc­ tion and the fossil record of the arthropods, In: C . P . Larwood, (ed . ) Extinction and survival i n the fossil record. Systematics Association Special Volume No. 34, pp. 171 - 209 . Clarendon Press, Oxford. Cope, J . C.W. & Skelton, P.W. (eds) 1985 . Evolutionary case histories from the fossil record. Special Papers in Palaeontology No. 33 . Cracraft, J. & Eldredge, N. (eds) 1979 . Phylogenetic analysis and paleontology. Columbia University Press, New York Fortey, R.A. & Jefferies, R.P.5. 1982. Fossils and phylogeny a compromise approach . In : K.A. Joysey & A. E . Friday (eds) Problems of phylogenetic reconstruction . Systematics Association Special Volume No. 21, pp . 197-234. Hennig, W. 1966 . Phylogenetic systematics . University of Illinois Press, Urbana. Hill, c.R. & Camus, J . M . 1986 . Evolutionary cladistics of marattialean ferns . Bulletin of the British Museum (Natural History), Botany Series 14, 219-300 . Patterson, C. 1981 . Significance of fossils in determining evolutionary relationships . Annual Review of Ecology and Systematics 12, 195 - 223 . Patterson, C. & Smith, A . B . 1987. Is the periodicity of extinc­ tion a taxonomic artefact? Nature 330, 248- 252. Wiley, E . O . 1981 . Phylogenetics: the theory and practice of phylogenetic systematics . Wiley Interscience, New York.

5 . 2 . 2 Cladistics P . L . F O RE Y

Introduction Cladistics is a method of biological classification which, in its purest form, seeks to group taxa into sets and subsets based on the most parsimonious distribution of characters . The results of analysis are expressed in cladograms which are atemporal (Fig. tB, left) showing only the distribution of characters and representing a general pattern with which several evolutionary trees might be compat­ ible . A highly readable contemporary account is given by Wiley (1981) . Cladistic methods were orig­ inally formulated by Hennig (1966) under the name 'Phylogenetic systematics' . Hennig explained his ideas within an evolutionary framework. This ac­ count treats cladistics in an historical way, leading from its evolutionary formulation to the more general theory. Hennig' s contribution was to offer a precise definition of relationship and to outline how re­ lationship might be detected. Hennig's concept of relationship is relative and is illustrated in Fig. lA. Taxa B and C are more closely related to each other than either is to a third taxon, A, because B and C share a common ancestor, X at time t2, not shared with any other taxon . Similarly A is more closely related to B + C than to D because these taxa share a unique common ancestor, Y at time t1 . B and C are called sister-groups; A is the sister-group of the combined taxon B + C . The aim of cladistic analysis is to search for the sister-group hierarchy, and express the results in branching diagrams called cladograms .

Synapomorphy, symplesiomorphy and autapomorphy Sister-groups are discovered by finding shared derived characters (synapomorphies) inferred to have originated in the latest common ancestor. Synapomorphies can be thought of as evolutionary novelties or as homologies . From Fig. lA characters 3 and 4 are synapomorphies suggesting that the lizard and the salmon shared a unique common ancestor X at time t2 • Shared primitive characters (symplesiomorphies) are characters inherited from more remote ancestry and are irrelevant to the

5.2 Analysis of Taxonomy and Phylogeny

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problem of relationship of the lizard and the salmon . Thus, the shared possession of characters 1 and 2 in the salmon and the lizard would not imply that they shared a unique common ancestor because these attributes are also found in the shark. Characters 1 and 2 are more universal and may be useful at a higher hierarchical level to suggest common ancestry, Y at time tl . lt is important to recognize that synapomorphy and symplesiomorphy describe the status of charac­ ters relative to a particular problem . Thus, characters 3 and 4 are synapomorphies when one is interested in the relationships of the salmon or the lizard, but symplesiomorphies if the problem involves the relationships of different species of lizards or dif­ ferent species of salmon . Hennig recognized a third

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distribution: those characters unique to one species or group, such as characters 5 - 9 in the lizard, 10 in the salmon, 11 in the shark, and 12 in the lamprey. These he called autapomorphies, which in Fig. lA define the terminal taxa A -D . The characters used to discover relationship are derived characters or character-states and this implies acceptance of transformation (absence � presence, or condition a � a ' ) . Hennig suggested several criteria by which polarity of transformation may be recognized. The two most frequently used are ontogenetic transformation and outgroup analy­ sis (see Ax 1987) . The latter is most applicable to palaeontological studies, and may be briefly stated: when a character exists in a variable state within the group under study, the condition that is also

432

5 Taxonomy, Phylogeny, and Biostratigraphy

found outside the group is the plesiomorphic state . Cladistic analysis is concerned with ordering these derived states into transformation series and this is done by choosing the arrangement of taxa that is congruent with the greatest number of characters . An alternative way of expressing this is that the most parsimonious solution is sought. There are a number of computer algorithms available to help in this task (Platnick 1987) . It has been argued that it is inappropriate to apply the principle of parsimony to an exercise seeking to reconstruct phylogenetic relationship; after all, evolution may not have followed the most parsimonious course . In cladistic analysis the most parsimonious solution is sought because this is the qnly universal criterion by which different hypoth­ eses of relationship might be evaluated . This has been dubbed methodological parsimony . To accept a solution which is other than parsimonious re­ quires additional assumptions which themselves require independent justification . Types of groups

As a result of the relative definition of relationship, Hennig identified three types of groups: 1 A monophyletic group contains the latest common ancestor plus all and only all its descendants . In Fig . lA such groups would be BC(X), ABC(Y), DABC(Z) . In the particular example the mono­ phyletic groups would be called Osteichthyes, Gnathostomata and Vertebrata respectively . 2 A paraphyletic group is one remaining after one or more parts of a monophyletic group have been removed. Group AB (Pisces) is a paraphyletic group : one of the included members (B) is genealogically closer to C which is not part of the group Pisces. 3 A polyphyletic group is one defined on the basis of convergence, or by non-homologous characters assumed to have been absent in the latest common ancestor . A group AC containing the shark and the lizard, based on the possession of internal fertili­ zation would be considered a polyphyletic group . Internal fertilization is certainly a derived character within vertebrates and might be indicative of a monophyletic group . But a grouping based on this feature is not congruent with any other character distributions . Rather, it is incongruent with a group BC suggested by two characters (3, 4) . A polyphyletic group represents a non-parsimonious solution, and the characters by which we recognize it are non­ homologous, false guides to relationship . Most systematists would agree with the desir-

ability of recognizing monophyletic groups and re­ spect the artificiality of polyphyletic groups. It is paraphyletic groups which are the source of debate, particularly with palaeontologists . Paraphyletic groups

Cladistic classification insists that only monophy­ letic groups be included, as recognized on the basis of synapomorphy . Paraphyletic groups obscure re­ lationships because they are not real in the same sense, they do not have historical reality and they cannot be recognized by a synapomorphy. Reptilia, for instance, is a paraphyletic group recognized by having synapomorphies (amniotic membranes, cleidoic egg) of a larger group (Amniota) but lack­ ing the synapomorphies of two contained amniote subgroups - birds (feathers) and mammals (hair) . Reptiles are distinctive only because they lack characters . The 'defining attributes' of such a para­ phyletic group are symplesiomorphies (shared pri­ mitive features) only . Evolutionary classification (Section 5 . 2 .3) allows the inclusion of paraphyletic groups with the justifi­ cation that extra evolutionary information is conveyed. That extra information is seen to be evo­ lutionary divergence . From Fig. lA then, evo­ lutionary systematists consider it justified to retain Pisces as a paraphyletic group and separate off the lizards (Tetrapod a) in a collateral group to empha­ size the many autapomorphies (characters 5 9 ) of this latter group . In a cladistic classification such divergence would be expressed through the number of autapomorphies . Paraphyletic groups are popular i n palaeontology (Patterson 1981) because they are traditionally the ancestral groups (fishes ancestral to tetrapods, rep­ tiles ancestral to birds and mammals, inarticulate brachiopods ancestral to articulates, regular echin­ oids ancestral to irregular echinoids) . These para­ phyletic groups are based on absence of characters of the presumed descendants . The problem is compounded in fossils because conditions of soft anatomy used in the classification of Recent rep­ resentatives cannot be checked; nor can it ever be certain whether absence of features is real or a preservational artifact. In other words, nothing can be found to support an ancestrallparaphyletic group . A special case of ancestral/paraphyletic groups frequently occurs in palaeontology: the extinct, presumed ancestral group . Hennig calIed these stem-groups, and well known examples include -

5.2 Analysis of Taxonomy and Phylogeny Rhipidistia, Cotylosauria, Pelycosauria, and Ther­ apsida . All of these groups are paraphyletic, and are defined on the absence of features of the presumed Recent descendants . When analysed in a cladistic fashion, such groups usually turn out to be com­ posed of successively more derived taxa (some showing more synapomorphies with the Recent group) . Thus, a stem-group to the Euechinoidea, such as the Palaeozoic 'Perischoechinoidea', can be resolved into a series of sister-group relationships of increasingly derived taxa (Smith 1984) . By break­ ing up such a paraphyletic group into real historical entities (successive monophyletic taxa) some insight is gained into the sequence of character acquisition, from which may be deduced something about bio­ logical evolution . The use of paraphyletic groups also introduces problems when trying to express ideas of relation­ ship in a Linnaean taxonomy . Paraphyletic groups such as Reptilia and Inarticulata have equal rank with their presumed descendants (A ves and Mam­ malia, Articulata) in an attempt to emphasize the morphological divergence of the descendants . This implies that all members of the Reptilia are each other's closest relatives . But this is not so since, amongst reptiles, crocodiles are known to be closer to birds than to lizards or turtles . Paraphyletic groups therefore introduce an asymmetry between the Linnaean classification and ideas of phylogeny .

Cladistics and Linnaean classification It is for these reasons that cladists try to apply equal rank to sister-groups . For cladists the classification and the cladogram are the same thing. The Linnaean classification for Fig. lA would be : Group ABCD Subgroup D Subgroup ABC Infragroup A Infragroup BC B C It has been mentioned above that for many fossil groups currently thought of as paraphyletic stem­ groups, it may be possible to divide them into a series of successively more cladistically derived taxa. Potentially, this could provide problems because, to express every sister-group pairing, a very large number of ranks might be needed . There are, how­ ever, several conventions that can be adopted to circumvent this problem (Wiley 1981) including the

433

use of a rank plesion for fossil taxa (Patterson & Rosen 1977) .

Cladograms and trees Cladistic classification, as explained so far, is con­ cerned with searching for sister-groups and express­ ing the results of that search in classifications where sister-groups are given equal rank. When Hennig formulated his phylogenetic system he did so in strictly evolutionary terms . His branching diagrams were phylogenetic trees with an implicit time axis in which hypothetical ancestors were located at the nodes; the nodes represented speciation or cladogenetic events with evolutionary transform­ ation taking place along the branches. It soon became apparent, however, that Hennig's phylo­ genetic trees or cladograms were more general than originally thought. It is possible to view a diagram such as Fig . lA as a strict cladogram, with no time axis, representing instead a pattern of distribution of characters . The nodes denote a hierarchy of synapomorphies and the relationship can be represented as a Venn dia­ gram of sets and subsets in which there is no implication of ancestry and descent (Fig. lB) . Given the character information contained in this Venn diagram, there are a number of equally compatible evolutionary trees that embody the concepts of an­ cestry and descent with modification . Five such trees are shown in Fig. lB (right) . One, and only one, has the same topology as the cladogram and this is the one in which the nodes represent hypo­ thetical ancestors . The others contain one or more real ancestors . Choice between these trees depends on factors other than the distribution of characters, which is the only empirical content . Selection of one tree in preference to others may depend on a willingness to regard one taxon as ancestral to the others . Alternatively, the possibility of certain trees involving real ancestors might be denied because of an unfavourable stratigraphic sequence . The im­ portant point is that while evolutionary trees are very precise statements of singular history, their precision is gained from criteria other than character distributions; these trees cannot be justified on characters alone . It is possible that stratigraphic data, combined with independent stratigraphic testing (assessments of completeness and suitability of sedimentation) may restrict the choice of trees . Cladograms, on the other hand, are statements of general pattern testable by applying more data and are useful for, amongst other tasks, the analysis of

5 Taxonomy, Phylogeny, and Biostratigraphy

434

biogeographic history (Nelson & Platnick 1981; Sec­ tion 5.4) .

References Ax, P. 1987. The phylogenetic system . Wiley Interscience, New York. Hennig, W. 1966 . Phylogenetic systematics . 2nd edn . 1979. University of Illinois Press, Urbana. Nelson, G. & Platnick, N. 1981 . Systematics & biogeography: cladistics and vicariance. Columbia University Press, New York. Patterson, C. 1981 . Significance of fossils in determining evolutionary relationships . Annual Review of Ecology and Systematics 12, 195 - 223 . Patterson, C. & Rosen, D . E . 1977. Review of ichthyodectiform and other Mesozoic teleost fishes and the theory and practice of classifying fossils. Bulletin of the American Museum of Natural History 158, 81 - 172 . Platnick, N . ! . 1 987. A n empirical comparison o f microcom­ puter parsimony programs . Cladistics 3, 121 - 144 . Smith, A.B . 1984. Echinoid palaeobiology. George Alien & Unwin, London. Wiley, E . O . 1981 . Phylogenetics: the theory and practice of phylogenetic systematics . Wiley Interscience, New York.

5 . 2 . 3 Evolutionary Systematics A . J . CHARIG

species hierarchically - into nested sets - accord­ ing to their possession of characters held in common (shared characters) . The characters used were essen­ tially anatomical . Such a procedure was generally easy when the only species considered were those living today, most of which are clearly definable through their genetic isolation . But the discovery of fossil forms that were intermediate in their charac­ ters between two or more extant groups, coupled with the general acceptance of the concept of organic evolution, together led systematists to change their purely typological approach into something more 'evolutionary' . It seemed reasonable to base the classification upon phylogenetic (i. e . genealogical) relationships : the closer the phylogenetic relation­ ship between two species, the closer should they be to each other in the classificatory hierarchy . Thus the assessment of phylogenetic relationships was still based mainly, if not exclusively, upon characters held in common . However, it is clear that hierarchies constructed upon different shared characters are often incom­ patible with each other. It is therefore logically im­ possible that all shared characters indicate a close phylogenetic relationship; in some cases apparent identity of characters must be due to homoplasy (parallelisms, convergences and reversals) and can have little phylogenetic significance . Recognition of the phylogenetically correct hierarchy may be as­ sisted by determination of the polarity of evo­ lutionary trends and by choosing the hierarchy that appears most frequently (maximal congruence or parsimony) .

Introduction

Phylogeny and classification

'Evolutionary systematics' should not be confused with 'phylogenetic systematics' . It is an accident of history that the words 'evolutionary' and 'phylogen­ etic', despite their virtual synonymy, have come to be associated with two very different methods of reconstructing phylogeny and classifying organ­ isms . Charig (1982) recognized this as a possible source of confusion and misunderstanding and suggested that the generally applied evolutionary approach, otherwise called 'conventional' or 'ortho­ dox', might instead be referred to by the wholly non-descriptive but also wholly unambiguous name 'Simpsonian systematics' ; this was intended to be a tribute to the late G . G . Simpson, once the leading exponent of that approach . Early classifications of biological organisms, exemplified by that of Linnaeus, arranged the

At this point it is important to ensure that the distinction between phylogeny and classification be clearly understood . Phylogeny is the history of the evolution of living organisms; it is the pattern of the evolutionary pathways by which the millions of organic species, past and present, have arisen . It is an objective reality; the organisms actually evolved in a particular way. Yet our knowledge of phylogeny is very imperfect; our attempted reconstructions of it may differ greatly from each other, and we cannot be sure which (if any) is correct . Classification, on the other hand, is the ar­ rangement of living organisms into a meaningful and practical hierarchy, a system of reference . It need not be connected with the phylogeny in any way. It should permit the cataloguing of organisms (in, say, a museum collection or a textbook), assist

5.2 Analysis of Taxonomy and Phylogeny the memory and enable the prediction of certain attributes; it may also, though not necessarily, indi­ cate the presumed phylogenetic relationships . It is entirely man-made and subjective, so that systems of classification may vary between authorities even more than do the attempted reconstructions of phylogeny. The only connection between phylogeny and classification is the fact that the two forms of classifi­ cation most commonly used today, the evolutionary and the stratophenetic, are based primarily upon the perceived phylogeny; and it is obvious that the stratophenetic approach (Section 5 . 2.4) can be used only by palaeontologists . Also based on phylogeny, but exclusively on that, are certain varieties of cladistic classification - the 'phylogenetic sys­ tematics' of Hennig (1966) and the 'phylogenetics' of Wiley (1981); their practitioners will be referred to below as 'phylogenetic cladists' . In contrast, 'transformed cladistics' (Platnick 1980) (now more usually called 'pattern cladistics' ; Beatty 1982) does not even require that evolution should have taken place (Section 5 . 2 . 1) ; nor do phenetic classifications . The making of an evolutionary classification therefore consists of two major stages: the recon­ struction of the phylogeny and, based on that phylogeny, the actual setting up of a formal classification.

Reconstruction of phylogeny Phylogeny is represented graphically as a den­ drogram ('family tree') . Parts of the tree will probably remain unknown, with unresolved polytomies, and our knowledge of much of the rest is likely to be - to a varying extent - uncertain. There are, essentially, two ways of reconstructing it. One is by analysing the distribution of characters among the species concerned (' cladistic analysis', the basic method used by phylogenetic cladists; Section 5 . 2 . 2) . The other is by analysing the distri­ bution of species in the strata (the basic method employed by stratopheneticists, who of course in­ clude in their ranks only palaeontologists; Section 5 . 2 .4) . However, the phylogenetic cladist is generally prepared to confirm and/or supplement his cladistic analysis with stratophenetic evidence, and vice versa; further, both the phylogenetic cladist and the stratopheneticist may obtain additional evidence on the phylogeny from the embryology and on­ togeny of extant organisms, and from the geographi­ cal distribution of organisms both Recent and fossil . (It should be noted that there are some cladists who,

435

in their attempted reconstruction of the phylogeny, consider it improper to supplement or confirm the cladistic analysis in any way . ) Evolutionary system­ atists resemble the less doctrinaire cladists in that they use a judicious combination of both basic methods, with character distribution analysis as their primary method; thus, if the data permit, they will confirm and supplement their results by means of evidence from the fossil record (i . e . stratophene­ tically), from embryology and ontogeny, and from geographical distribution. It must be said that, in the past - when all systematists might have been described as 'evo­ lutionary' - they were not rigorous enough in their application of character distribution analysis; they often tried to unite two groups as 'sister-groups' (i. e . originating from an immediate common ances­ tor) on the evidence of shared characters that were sadly inappropriate . The characters were sometimes 'primitive', what the cladists call plesiomorphous, and were therefore found in other (or even all) mem­ bers of the group in question. They might some­ times have been homoplastic, with their presence in the two groups being due to parallelism, convergence or an evolutionary reversal, rather than to an im­ mediate common ancestry . Although such problems may often be clarified by a demonstration of polarity or maximal congruence, that had not been done . Reductions and losses, frequently employed as shared characters, could be included here as possible cases of homoplasy; it is only rarely that reductions can be compared to ascertain precise similarity, and losses never . Further, shared characters were some­ times vague and ill-defined, or too broadly defined to be used properly as indicators of close phylogen­ etic relationship (e . g . 'warm-blooded') . Unfortu­ nately many present-day phylogenetic taxonomists, of both schools, are still guilty of such sloppy work.

Erecting a classification The second component of evolutionary systematics, the actual setting up of a formal classification, con­ sists of the arbitrary division of the phylogenetic tree into segments, sub segments and so on; each segment constitutes a taxon, the origin of which is defined by the first appearance of an evolutionary novelty (Fig. 1 ) . Thus the Class Reptilia begins with the first appearance of the amniote egg. Some of the radiating lineages within that class have become entirely extinct (e .g. Ornithischia, Ichthyosauria) while others have survived to the present day (e . g . Testudinata, Squamata) . Yet other lineages (e . g .

436

5 Taxonomy, Phylogeny, and Biostratigraphy Present da y

100

200

300 Ma

Fig. 1 A greatly simplified family tree (,spindle diagram') of the Amniota. Paraphyletic taxa are dash-stippled and named in lower case lettering. Each gives rise to at least one other taxon. Not named on the diagram are : Reptilia everything except Aves and Mammalia; Archosauria Thecodontia + all descendant groups except Aves; Synapsida Pelycosauria + Therapsida. Holophyletic taxa are dot-stippled and named in upper case lettering. They give rise to nothing else . =

=

=

Theropoda, Therapsida), however, have evolved into forms so different that the part of the lineage in question is subjectively considered to merit place­ ment in separate classes (Aves, Mammalia respec­ tively), the initiation of each being marked by the first appearance of its own characteristic evolution­ ary novelty . Thus the reptiles may be defined as tetrapods that possess an amniote egg but have not yet acquired either a functional dentary-squamosal jaw articulation (the possession of which defines a mammal) or feathers (defining birds) . This means that a taxon of given rank may be deemed to have evolved from another taxon of the same rank, so that Class A may be regarded as ancestral to Class B . A corollary of this is that Class A, since it does not include Class B, does not include all its own descendants, i . e . it is not a complete clade; it is not holophyletic (Ashlock 1971 ; 'mono­ phyletic' sensu Hennig) but is paraphyletic. All stem=

groups, all ancestral groups are ipso facto paraphyle­ tic; good examples are Reptilia (excluding Mam­ malia and Aves), Synapsida (excluding Mammalia), Archosauria (excluding Aves) and Thecodontia (ex­ cluding all other archosaurs) . Cladists abhor and deride paraphyletic taxa, saying that they 'cannot be characterized' , do not have historical reality', and 'obscure close relationships' (see, for example, Section 5 . 2 . 2); they forget that the relationship is 'close' only if it be defined in cladistic terms! Evo­ lutionary systematists, on the other hand, consider that paraphyletic taxa can be characterized (in mathematical parlance, as 'complement sets') and they find them extraordinarily useful, especially when discussing ancestry. The seemingly endless argument over the desir­ ability or otherwise of admitting paraphyletic taxa into the classification is, in fact, the old argument over the relative merits of the 'horizontal' and 'vertiI

5 . 2 Analysis of Taxonomy and Phylogeny cal' classifications, to which there can be no defini­ tive solution . When a radiating group is split into its separate components, should a 'stem-group' be left at the base of the radiation, or should the split be extended as far back as possible towards the origin of the group? Alternatively, putting the prob­ lem into human terms : to whom is one more closely related, a first cousin, or a direct descendant a hundred generations on? The evolutionary system­ atist's answer is the first cousin, the cladist's is the direct descendant - no matter how many gener­ ations removed. It all depends, of course, on the meaning attached to 'relationship' . But at least it cannot be denied that one shares a much greater proportion of genetic material with the first cousin.

Advantages and disadvantages of evolutionary systematics The method of phylogeny reconstruction used by evolutionary systematists is much the same as that used by phylogenetic cladists (it employs all the available evidence, of whatever category); it differs from it mainly in that there is no requirement to force a series of dichotomous resolutions from every multiple split, even where the available evidence does not justify such resolution. In the past, alas, the method has generally been applied too loosely, too unscientifically; and even today, all too fre­ quently, the same is still true . However, provided that it is used with proper intellectual rigour, as advocated by Hennig, the method is still the best available . This method of classification possesses several advantages over the now fashionable cladistic method . It is essentially the most practical method, the most useful for a wide variety of purposes, and it contains the greatest amount of information; one might instance the hiving-off from a large taxon (e . g . Reptilia) of a daughter-group (Aves) into a separate taxon of equivalent rank (Class) in order to indicate extreme evolutionary divergence . (It is true that this to some extent obscures the simple phylo­ genetic content of the classification, but that infor­ mation is still available, in unambiguous graphic form, in the dendrogram. ) The structure of the evo­ lutionary classification permits the discussion of ancestor- descendant relationships, whereas cladistic classifications regard all taxa as terminal in position and consider only sister-group relation­ ships . Moreover, the very fact that evolutionary classifications are drawn up in an arbitrary fashion confers upon them the necessary degree of uniform-

437

ity and stability that is lacking in cladistic classifi­ cations; the latter vary enormously from worker to worker and, according to the cladistic creed, they are obliged to change with every alteration to the perceived phylogeny. Finally, there is the important point that evolutionary classifications are used far more widely than any other.

References Ashlock, P . D . 1971 . Monophyly and associated terms. Systematic Zoology 20, 63- 69 . Beatty, J . 1982 . Classes and cladists . Systematic Zoology 31, 25- 34 . Charig, A . J . 1982. Systematics i n biology: a fundamental comparison of some major schools of thought. In: K.A. Joysey & A . E . Friday (eds) Problems of phylogenetic recon­ struction . Systematics Association Special Volume No. 21, pp . 363-440. Hennig, W. 1966 . Phylogenetic systematics . 2nd edn 1979 . University o f Illinois Press, Urbana. Platnick, N . ! . 1980. Philosophy and the transformation of cladistics. Systematic Zoology 28, 537-546 . Wiley, E . O . 198 1 . Phylogenetics: the theory and practice of phylogenetic systematics . Wiley Interscience, New York.

5 . 2 . 4 Stratophenetics P . D . G I N G E RI C H

Stratophenetic analysis i s an approach to under­ standing the ancestor- descendant or genealogical relationships of organisms and groups of organisms preserved in the fossil record . The approach is based on: (1) quantitative assessment of morphological (phenetic) similarity, interpreted in the context of (2) independent evidence of geological age (fur­ nished by stratigraphy) . Morphology is import­ ant because it is what we can see and study directly in living organisms, and the material record of life in the past is morphological . Time is important because genealogy is sequential. Stratigraphy is the discipline that correlates short sequences of life's history ordered by superposition in local geological sections, building longer composite histories for continents and seaways . Geography too plays a role in phylogenetic inference because organisms pro­ pagate within the spatial confines of their geo­ graphical ranges .

438

5 Taxonomy, Phylogeny, and Biostratigraphy

The goal of stratophenetics, like that of cladistics (Section 5 . 2.2), is more than a phenetic assessment of affinity or a classification of organisms based solely on morphological similarity. Stratophenetics and cladistics both seek to clarify genealogical relationships . Stratophenetics differs from cladistics in placing more emphasis on time and in seeking ancestor- descendant relationships explicitly. These are expressed in phylogenetic trees rather than cladograms. The ultimate goal is to know the history of life . It is sufficient, in the interim, that strato­ phenetics continues to augment and extend a well established outline of this history based on fos­ sils, identifying gaps as well as continuity in the historical record .

General approach The term stratophenetic(s) was coined to characterize palaeontological procedures commonly used in studying phylogenetic relationships in the fossil record (Gingerich 1976, pp . 15- 16) . These pro­ cedures were long employed without a name (see Colbert 1963; Rowell 1970; and others) because the logic seemed self-evident and no competing ap­ proaches were advocated by palaeontologists . Responding to the development of phenetics and cladistics by neontologists, Simpson (1976) listed a summary of 'eclectic' or 'evolutionary' systematic procedures, but Simpson's procedures and indeed the names he used to describe them seem unduly broad and vague (but see Section 5 . 2.3) . A stratophenetic approach to phylogeny involves four steps: 1

Within-locality

or

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organization .

Quantitative study of morphological variation in each locality sample of the organisms under study, to identify clusters of specimens belonging to species or other operational taxonomic units (populations, genera, families, etc . ) based on mor­ phological similarity at one time and place . A taxon exists only in relation to another, and each taxon in a given time interval or locality must differ by a measurable amount from all others before it can be recognized as distinct . 2 Stratigraphic organization . Superposition of lo­ calities within local stratigraphic sections and cor­ relation of localities between sections . Correlation is based on sequential change observed in fossils, palaeomagnetic signatures, radiometric dating, and any other geological evidence . Stratigraphic superposition determines the polarity of character

transformations observed in a sequence of fossils . Superposition in each local section is determined before correlation between sections. Thus super­ position and polarity are independent of correlation . 3 Stratophenetic linking. Operational taxonomic units in adjacent time intervals are linked together by their overall morphological similarity, beginning with intervals that have the most taxonomic units and linking those in subjacent (earlier) or super­ jacent (later) intervals . When a taxon overlaps no other in an adjacent interval, the search for a similar ancestor or descendant is extended to the next sub­ jacent or superjacent interval, and this process may be repeated . Ideally, there is more overlap in the ranges of variation of taxa linked between two adjacent intervals than there is in the ranges of variation of taxa within the same interval . No attempt is made to restrict similarity to shared derived features at this stage because there is no way to determine a priori which characteristics are primitive and which are advanced, and there is no way to determine a priori which advanced features are uniquely derived and which evolved convergently. Stratophenetic linking can be approached, as Rowell (1970) has done, by looking at species in a multivariate morphometric space with principal component I (or I and 11) as a horizontal axis (or axes), lifting species to their appropriate strati­ graphic levels on a vertical axis, and drawing con­ nections between similar forms in successive intervals of time . The most economical pattern of linking is the one requiring the minimum number of evolutionary lineages connecting all taxa, and the most complete pattern is the one with the fewest empty intersections of a lineage passing through a time interval . 4 Hypothesis testing. Patterns of stratophenetic link­ ing are phylogenetic hypotheses that are tested each time a new specimen, a new locality sample, or a new taxon is discovered that belongs to the group under study . Robust patterns are those that change little as new discoveries are made . Classification based on phylogeny requires two additional steps:

5 Grouping. Operational taxonomic units are grouped into sets of similar forms corresponding to higher taxonomic units (genera, families, etc . ) . These groups are constrained t o include all intermediates in the minimum spanning tree of stratophenetic linking . 6 Diagnosis : Groups are distinguished from each

5 . 2 Analysis of Taxonomy and Phylogeny other using combinations of characteristics unique to each group . Shared derived characteristics are particularly important in diagnosing groups from ancestral stocks that preceded them in time . Shared derived diagnostic characteristics are identified a posteriori by their distribution on the minimum spanning stratophenetic tree .

representing all species-level taxa within each fossil-bearing locality; stratigraphic organization involves correlating all localities bearing the same or closely similar taxa and arranging these in strati­ graphic order for comparison . Phenetic linking of similar species-level taxa in adjacent intervals is shown with dashed lines in Fig. 1 . The result suggests that there is a single carpolestid lineage and a single plesiadapid lineage below 500 m, while two carpolestid daughter lin­ eages and two plesiadapid daughter lineages are present in some intervals above 500 m. Each pattern is economical in that the relationships of all species in each family require no more lineages than the maximum number of coexisting taxa; and each pat­ tern is reasonably complete in that there is only one extended interval (800- 1200 m) where lineages lack representative specimens or intermediate taxa. The patterns shown in Fig. 1 are tested every time a new carpolestid or plesiadapid is found in north­ western Wyoming. There have been c. 80 new specimens found since 1976. These are super­ imposed in Fig. 1 as solid circles and associated integers . All fall within or near the dashed lines of the original patterns of linking, indicating that the original stratophenetic hypotheses of relationship

Stratophenetic linking at the species level Within-locality organization, stratigraphic organ­ ization, phenetic linking, and hypothesis testing are all illustrated in Fig . 1, which outlines the North American radiation of eight species of Carpolestidae and nine species of Plesiadapidae (archaic primates) found in a 1400 m stratigraphic section on Polecat Bench (and shorter sections meas­ ured nearby) in northwestern Wyoming . Solid lines represent the means and probable ranges of seven­ teen species-level taxa (Elphidotarsius jlorencae, Pronothodectes jepi, etc . ) recognized in studies by Rose (1975) and Gingerich (1976) . Species differ principally in size, but they also differ in other morphological characteristics (dental formula, enamel crenulation, incisor form, etc . ) . Within­ locality organization involves grouping specimens Wa, Ch

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Pattern of stratophenetic linking in early Cenozoic Carpolestidae and Plesiadapidae. Evolution of tooth size (logarithm of length multiplied by width of first lower molar) and, by inference, evolution of body size (estimated weight in kilograms) are given on the horizontal axis, but the pattern of linking shown here is based on all characteristics preserved in carpolestid and plesiadapid fossils. The vertical axis is a metre level in one master stratigraphic section in northwestern Wyoming (U.S.A.). Standard subdivisions of the Palaeocene and Early Eocene time-scale are also shown. The phylogenetic hypothesis shown here has proved to be robust in that new discoveries (solid circles and associated integers representing multiple specimens) have required little change in the basic pattern of linking. (From Gingerich 1976, 1980, with additions . ) Reproduced, with permission, from the Annual Review of Earth and Planetary Science, Vol . 8 © 1980 by Annual Reviews Inc .

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are robust and require little modification to ac­ commodate the new evidence found to date . It is worth noting that the patterns of strato-

phenetic linking shown here are divergent upward, L e . contemporary lineages are found to join at their bases rather than their tops. The important and

5 . 2 Analysis of Taxonomy and Phylogeny long-known generalization that phylogenetic trees diverge rather than converge through time is an empirical result of stratophenetic analysis .

Stratophenetics and cladistics at higher taxonomic levels Stratophenetics and cladistics can be viewed as alternative approaches to the reconstruction of phylogeny. Which approach is more appropriate in any particular instance depends on the nature of the historical record available for the group under study. Where there is a dense and continuous fossil record available for a group of closely similar species, like the example discussed above (Fig. 1), it is appropriate to analyse the evidence strato­ phenetically. Numerous intermediate forms provide evidence of transition, and the taxa differ in so few characteristics that it would be difficult to make meaningful cladistic inferences. At the opposite end of the spectrum, there are groups of organisms (e . g . some insects, bony fishes, perching birds) for which the fossil record is notably discontinuous and includes only a fraction of the morphological diversity observed to be living today. Here stratophenetic analysis can contribute little, and cladistic inference may be warranted . Cladistic inference is rarely carried out in a vacuum, however, and it is usually appropriate to structure inferences to take advantage of broad outlines of relationship evidenced in the fossil record . The evolutionary diversification of the mam­ malian order Primates (Fig. 2) is an example where the phylogenetic tree obtained from stratophenetic linking provides only an outline of the history of the group . Genera illustrating each of the seven superfamilies of living primates are arranged across the top of the diagram . Genera known from skulls in the fossil record, representing one of the living superfamilies or one of three extinct superfamilies, are positioned beneath their most similar living relatives in the appropriate interval of geological time . Stratophenetic linking based on all the evi­ dence of morphological similarity (dashed lines) shows likely genealogical relationships at the family or superfamily level. Of the living groups, Tupaioidea may be related to Microsyopoidea and Plesiadapoidea, but there is a very large gap in their fossil record . Tarsioidea extend back into the Eocene (to Necrolemur and its allies), but here again there is a very large gap in the Late Cenozoic. Cercopithecoidea, Hominoidea, and Ceboidea have a reasonably dense fossil record in the Late

441

Cenozoic, and they appear to converge on Apidium­ like and Aegyptopithecus-like forms in the Middle Cenozoic. Lorisoidea and Lemuroidea have poor fossil records, and they may or may not be derived from Eocene Adapoidea. Consideration of all the morphological and geo­ graphical evidence in a stratigraphic context ident­ ifies parts of the historical record that are better known than others; such consideration identifies areas of questionable relationship (origin of lemurs and lorises, for example) that may repay a cladistic analysis carried out in the context of a strato­ phenetically based outline of primate history (Gingerich 1984) . The scale is different, and the pattern of phylogeny is less complete, but the prin­ ciples of stratigraphic organization and phenetic linking used to produce the outline of primate phylogeny shown here are the same as those used to link species of Plesiadapis in Fig. 1 .

Conclusions Stratophenetics differs from cladistics in placing more emphasis on time and in seeking ancestor ­ descendant relationships explicitly. These relation­ ships may be at the species level, or more broadly drawn at higher taxonomic levels . Stratophenetics as a general approach to phylogeny at any taxonomic level seeks to identify taxa intermediate between others in form, in space, and in time, because inter­ mediates provide the only positive evidence that a given transition occurred. Stratophenetic outlines are phylogenetic trees constructed with time as an integral component . Phylogenetic trees are more informative than clado­ grams in relating the divergence of major taxonomic groups to geological time . In addition, strato­ phenetic outlines have heuristic value in identifying what we do not know (as well as what we know), thus identifying gaps in the historical record worthy of investigation. Time is a fundamental dimension in evolutionary studies, and a major goal of palae­ ontology should continue to be the study of the diversification of major groups of organisms in relation to geological time .

References Colbert, E . H . 1963 . Phylogeny and the dimension of time . American Naturalist 47, 319-331 . Gingerich, P. D. 1976 . Cranial anatomy and evolution of North American Plesiadapidae (Mammalia, Primates) . University of Michigan Papers on Paleontology 15, 1 - 140 .

5 Taxonomy, Phylogeny, and Biostratigraphy

442

Gingerich, P.D. 1980. Evolutionary patterns in early Cenozoic mammals. Annual Review of Earth and Planetary Sciences 8, 407-424. Gingerich, P.D. 1984. Primate evolution: evidence from the fossil record, comparative morphology, and molecular biology. Yearbook of Physical Anthropology 27, 57- 72. Rose, K.D. 1975 . The Carpolestidae, early Tertiary primates from North America. Bulletin of the Museum of Comparative Zoology, Harvard University 147, 1 - 74. Rowell, A.J. 1970 . The contribution of numerical taxonomy to the genus concept. In: E. L. Yochelson (ed . ) Proceedings

of the North

American

Paleontological

Convention

1,

264-293. Allen Press, Lawrence, Ka. Simpson, G . G . 1976. The compleat palaeontologist? Annual Review of Earth and Planetary Sciences 4, 1 - 13.

5 . 2 . 5 Problematic Fossil Taxa S . BENGTSON

Introduction Fossils that cannot readily be placed in established phyla or major groups are commonly called problematic. The main problem of problematic fossils (or 'problematica') has often been perceived as one of ignorance, suggesting that if we only understood the nature of such a fossil better we could place it in a living taxon, but recent work has emphasized the potential value of problematic fossils as possible representatives of extinct major taxa. They could thus expand our concept of the diversity of life beyond those clades that have survived to the pre­ sent day. A number of case studies and state-of-the­ art summaries were presented by Hoffman & Nitecki (1986) .

Extinct phyla If a phylum has become extinct, its fossils are re­ garded as problematic. The converse is not always true (i. e . problematic fossils are not necessarily representatives of extinct phyla), and the question of phylum affinity is one of the most fundamental that can be asked about such fossils . In general, there has been a reluctance to identify extinct phyla. The reasons for this seem to be linked mainly with a tendency to regard the now living assemblage of phyla as a fundamental division of the world of

organisms . This viewpoint is not necessarily valid . Nevertheless, it may be impractical to use the phylum concept for classification of organisms be­ longing to the earliest phases of radiation of major clades . Two aspects o f phyla should b e stressed . First, phyla themselves may be regarded as problematic taxa. They have come to circumscribe groups of organisms that are more or less obviously closely related to one another, the boundaries between phyla being drawn where the further relationship is unknown or uncertain. Second, phyla as currently recognized are almost exclusively based on living organisms . They are thus groupings of lineages that happen to have survived until now . Most fossil groups, even extinct ones, can be incorporated in such recent phyla with relative ease, and some may be admitted through a widening of the scope of a certain phylum. Problematic fossils are generally those that defy such straightforward taxonomic solutions; they become increasingly numerous with increasing geological age and are particularly characteristic of the Proterozoic and earliest Phanerozoic. This is consistent with the fact that all modern-day animal phyla appear to have been established no later than the beginning of the Phanerozoic .

Examples of problematic fossils Some major fossil groups in the Palaeozoic are classic problematic fossils . For example, conodonts and graptolites - both of considerable biostrati­ graphic importance - were for a long time re­ garded as taxonomic conundrums . Discoveries of fine anatomical structures - preserved soft parts of conodonts, and the so-called 'cortical bandages' in graptolite periderm - have brought the solution closer to a consensus on the chordate affinities of the former (Dzik in Hoffman & Nitecki 1986; Aldridge 1987) and the hemichordate affinities of the latter (Urbanek in Hoffman & Nitecki 1986) . Other well known examples of diverse fossil groups of uncertain affinities are archaeocyathans, hyoliths, and tentaculites . These are also of some biostratigraphic importance, albeit more limited than in the case of conodonts and graptolites . Archaeocyathans are a diverse group o f almost exclusively Lower Cambrian sedentary organisms typically forming a porous cup-shaped skeleton. They are usually considered as an extinct phylum, although their close similarity to sponges has re­ cently been emphasized (Debrenne & Vacelet 1983) .

5.2 Analysis of Taxonomy and Phylogeny Hyoliths and tentaculites had calcareous, cone­ shaped conchs that show some resemblances to mollusc shells . They are placed by some specialists in the Mollusca, but may be regarded more properly as representatives of extinct phyla. Most problematic fossils, however, are less di­ verse groups, sometimes represented only by a few species . Part of the reason for this may be artificial; rare fossils do not become intensively studied and are less likely to yield sufficient information to reveal their biological nature . But these problematic fossils may also represent clades of potential phylum status that did not survive to diversify. (Or, from a different viewpoint, they did not diversify enough to withstand chance extinction events . ) Many now living animals construct tubes a s more or less permanent living structures. Such tubes often have a very simple morphology and reveal little about the soft parts that formed them. The fossil record features a multitude of tubular fossils, and many of them are problematic fossils . The earliest known metazoan biomineralizer, the Late Precambrian Cloudina, built calcareous tubes . Towards the beginning of the Cambrian there appeared in rapid succession a large number of tube-dwelling organisms which constructed tubes of different substances, both purely organic and re­ inforced with agglutinating mineral particles or various biominerals . Some of these tubes are suf­ ficiently similar in form, composition, and structure to those of living organisms (such as annelids, pogonophorans, or foraminiferans) that a near af­ finity is probable, but in only a few cases are the similarities detailed enough for the affinity to be beyond reasonable doubt . Examples of well known problematic tubular fossils are the phos­ phatic hyolithelminths and the calcareous coleolids (cf. Fisher 1962) . Neither of these groups is demonstrably monophyletic. Many metazoan skeletons consist of numerous individual sclerites that normally dissociate upon the death of the animal . Such disarticulated fossils are another rich source of problematica throughout the Phanerozoic. The variety of skeletal elements in living organisms, however, is still very poorly known, and in some cases a closer comparison with spicules and sclerites of known organisms has been sufficient to solve the riddle of a problematic disjunct skeletal element . Nevertheless, a number of spicule- or sclerite-forming fossil organisms are sufficiently distinct in their mode of skeletalization that no homologies can be envisaged with known skeletal elements, and the organisms must be re-

443

garded as true problematica . Such fossils are particularly difficult to analyse, in that little infor­ mation on the body shape and anatomical detail of the animal can normally be gathered from the dis­ sociated sclerites, and no comparisons with better known related forms are possible . The occasional finds of complete articulated skeletons are of para­ mount importance in solving these problems . Spicular constructions characterize not only metazoans, but also metaphytes and protists . The skeleton of receptaculitids and cyclocrinitids consists of calcareous units radiating from an axis . These two groups are classic Palaeozoic problem­ atica that have drifted among metazoans (particu­ larly sponges), protists and metaphytes (particularly calcareous algae) in their search for a phylogenetic home . Current thought interprets them as calcareous algae, the cyclocrinitids being particularly close to the dasyclads (Nitecki in Hoffman & Nitecki 1986; Beadle 1988) . Calcareous algae have also been a popular 'home' for a large number of more or less nondescript calcareous structures, much to the despair of algologists (Babcock in Hoffman & Nitecki 1986) . Most of these fossils have been investigated only in petrographic thin sections, and the total morphology is poorly known, although their mineralogy may in fact be better understood than that of morphologically more distinct fossils. With the realization that many modern sponges (the coralline sponges, or 'sclerosponges') may in fact secrete basal calcareous skeletons, some laminated calcareous fossils (notably the stromato­ poroids) were with apparent success reinterpreted and reassigned from problematic coelenterate-like fossils to the sponges (Wood 1987) . Such a solution was also proposed by some workers for the tabulates, commonly regarded as corals . That the latter pro­ posal was over-enthusiastic has recently been demonstrated by the find of preserved polyps in a Silurian favositid (Copper 1985) . Micro- and nannofossils throughout the Late Pre­ cambrian and Phanerozoic include a large number of problematic remains . The organic microfossils include several diverse groups of considerable stratigraphic use but of unknown systematic affin­ ity . The acritarchs are an admittedly heterogeneous assemblage of cyst-like organic microfossils, thought to represent algal eukaryotes . They are uniquely important for biostratigraphy in the Pre­ cambrian, where fossils of biostratigraphic potential are otherwise almost absent. Chitinozoans are flask­ like, operculate, organic microfossils, often inter-

444

5 Taxonomy, Phylogeny, and Biostratigraphy

preted as the remains of metazoan eggs but in essence of unknown systematic affinity . They are known from the Cambrian to the Devonian and are of particular stratigraphic usefulness in the Lower Palaeozoic.

The analysis of problematic fossils When dealing with problematic fossils one is faced with a complex situation in which the most difficult problem may be to find a sufficient number of characters interpretable in terms of homology. Obviously there can be no strict formula to follow in order to assess whether a problematic fossil belongs to a certain phylum or not, but it may be helpful to use the following set of questions as a checklist: 1 What are the observable characters of the fossil? 2 What were the original characters of the animal when preservational and diagenetic factors have been taken into account? 3 What constructional and functional significance can be attributed to the characters? 4 Can these characters be interpreted as homolo­ gous to characters formed by members of any known phylum? 5 Are any of these possibly homologous characters unlikely to have arisen by convergence due to constructional or functional factors? 6 If a character cannot be, or is not likely to be, homologous with any characters in known phyla, can it be a derived character that evolved secondarily from a member of a known phylum? 7 Does the fossil show affinities with any other fossils from the same or any other period of time? Repeat questions 1 - 6 for this combined group . 8 If the fossil (group) can be interpreted on the basis of its characters as belonging to a known phylum, what are the consequences for the evo­ lutionary history of the phylum? 9 If the fossil (group) cannot be interpreted as belonging to a known phylum, what testable hy­ potheses may be formulated regarding its biological nature and phylogenetic origin? These steps do not outline a proper phylogenetic analysis but may serve as preparatory measures for one . Their main purpose is to serve as a safeguard against casual misidentifications .

should always attempt first to find a place for a problematic fossil in the known phylogeny of or­ ganisms, it is crucial to realize that the established taxonomic system is heavily biased towards the clades that have survived until today. The potential importance of extinct major groups is nowhere better illustrated than in the dichotomy between Glaessner (1984) and Seilacher (1984) in their inter­ pretation of the Late Precambrian Ediacaran biota (Sections 1 .3, 2 . 1 3 . 1) . Glaessner has championed a style of interpretation which assumes that this biota may be classified within the established taxonomic framework of living animals . Seilacher has argued that the Ediacaran biota represents a separate branch of multicellular organisms that became extinct at the end of the Precambrian. The two poles of the issue thus embody totally different understandings of the history of the animal kingdom. The dichotomy is more philosophical than methodological in nature, but any crucial test of the opposing concepts will have to take a large number of factors (taphonomic, preservational, physiological, behav­ ioural, etc . ) into account. Problematic fossils may thus be seen as challenges to our concepts of the diversity of the organic world in geological time . Whether they are problematic simply because we do not understand their nature sufficiently, or because they represent unknown branches of the evolutionary tree of life, they need to be studied with the utmost care and open­ mindedness . It is particularly important not to force a cosmetic solution onto the scientific problem that they present by simply assigning them to the least dissimilar known phylum.

References Aldridge, R.J. 1987. Conodont palaeobiology: a historical review. In: R.J. Aldridge (ed. ) Palaeobiology of conodonts, pp. 1 1 -34. Ellis Horwood, Chichester. Beadle, S . c . 1988 . Dasyclads, cyclocrinitids and recep­ taculitids: comparative morphology and paleoecology. Lethaia 21, 1 - 12 . Copper, P . 1985 . Fossilized polyps i n 430-Myr-old Favosites corals. Nature 316, 142 - 144 . Debrenne, F . & Vacelet, J . 1983 . Archaeocyatha: is the sponge model consistent with their structural organization? In: W.A. Oliver, W.J. Sando, S . D . Cairns, A . G . Coates, I . G . Macintyre, F . M . Bayer & J . E . Sorauf (eds) Recent

advances in the paleobiology and geology of the Cnidaria,

The significance o f problematic fossils Problematic fossils point to inadequacies in our interpretations of the fossil record . Although one

pp . 358- 369. Palaeontographica Americana, No. 54. Fisher, D.W. 1962. Small conoidal shells of uncertain affin­ ities. In: R . c . Moore (ed . ) Treatise on invertebrate paleon­ tology. W. Miscellanea, pp . W98-WI43 . Geological Society

5.3 Analysis of Taxonomic Diversity of America, Boulder, Co . , and University of Kansas Press, Lawrence, Ka. Glaessner, M.F. 1984. The dawn of animal life. Cambridge University Press, Cambridge. Hoffman, A. & Nitecki, M . H . (eds) 1986 . Problematic fossil taxa. Oxford Monographs on Geology and Geophysics No. 5, 267 pp. Oxford University Press, New York.

445

Seilacher, A. 1984. Late Precambrian and early Cambrian Metazoa : preservational or real extinctions? In: H.D. Holland & A.F. Trendall (eds) Patterns of change in Earth evolution, pp. 159 - 168. Springer-Verlag, Berlin. Wood, R. 1987. Biology and revised systematics of some late Mesozoic stromatoporoids. Special Papers in Palaeontology, No. 37.

5 . 3 Analysis of Taxonomic Diversity A . B . SMITH

Diversity enters into many aspects o f palaeobiology and particularly in the analysis of evolutionary pat­ terns and ecological (community) structure . In evol­ utionary studies taxonomic diversity is measured by counting or estimating the number of taxa of a specific categorical rank known from a particular locality, lithological formation or time-span, and is generally taken as a proxy for morphological diver­ sity . Ecological and biogeographical diversity are considered elsewhere (Sections 4. 10, 4 . 16, 4. 1 7) .

Species diversity A count of the number of species recorded from a rock unit or time-span will measure sampled diver­ sity (Fig. lA) . However, there are many reasons why sampled diversity may not be a true reflection of absolute diversity (Raup 1976), the following being some of the more important:

1 Sampled diversity correlates with the amount of rock available for study, measured either as surface outcrop area (Fig . Iq or estimated volume . The larger the outcrop area the greater is the diversity of species . However, surface outcrop area can only provide a crude approximation, since compilations do not distinguish between rocks of different facies . A large area of terrestrial Red Beds, for example, might have very much fewer fossils than a small outcrop of reefoidal limestone . 2 There is variation in the extent to which regional diagenesis and metamorphism destroy fossils from the rock record . 3 The number of palaeontologists involved in de­ scribing fossils from particular geological periods is

not uniform (Fig . 18); some time periods have at­ tracted more attention than others . Whether diver­ sity of species from specific time periods is directly related to the number of workers that have studied the rocks of that period, or whether the number of workers is proportional to the extent of rock outcrop is unresolved. The fact that most species are re­ corded from single localities or local areas (Smith & Patters on 1988) suggests that it is availability of surface outcrop of the correct lithofaces that is im­ portant . 4 The distribution of Lagerstatten (Section 3 . 1 1 ) affects apparent diversity . Deposits that preserve the soft-bodied biota provide a more complete glimpse of community structure and diversity . They create apparent peaks in diversity that are artifacts, produced because weakly skeletalized taxa are not preserved at other times; most workers avoid this problem by excluding such taxa from their analyses. In the analysis of global diversity through time, further biases may be introduced because of inaccu­ racies in the time-scale used (particularly crucial in normalized data), and the predominance of data from North America and Europe . All these problems have meant that the global history of species diver­ sity is difficult to reconstruct, even for specific groups . (See Padian & Clemens in Valentine 1986, for an excellent discussion of what can and cannot be deduced about changing diversities for the ter­ restrial habitat . ) Five different approaches t o estimating global species diversity through time have been proposed (see Signor in Valentine 1986, and the references therein) .

446

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be in equilibrium using this criterion, they con­ cluded that species richness could have been con­ stant since then . This conclusion was supported by Sepkoski's factor analysis of higher taxonomic groupings (Orders, Families) . 2 Empirical model (Fig . lE) . Valentine estimated the ratio of genera in families for each time period and

5.3 Analysis of Taxonomic Diversity then assumed that the same ratio held true for number of species in genera. Extrapolation from sampled generic diversity indicated that species diversity had increased by an order of magnitude since the middle Palaeozoic . 3 Species richness model (Fig . IF) . Bambach proposed that species richness could be estimated by looking at specific, well-preserved communities through time and extrapolating from them . From a hundred such communities he concluded that species diver­ sity was relatively stable during the Palaeozoic, but changed dramatically (particularly in nearshore habitats) after the Mesozoic . 4 Consensus model (Fig. I G) . Sepkoski and others combined diverse lines of evidence to produce a consensus model . They used sampled species, generic, familial, and trace fossil diversity, together with Bambach's within-habitat species diversity, and found a significant correlation between all five . The common element found was interpreted as signal. 5 Sampling model (Fig . IH) . Signor developed a method of estimating actual species diversity from sampling theory . He assumed that the frequency distribution of species at a particular geological horizon was log-normal . He used Raup's geological mapped area (Fig . Iq and estimated volume of rock, and Sheehan's estimate of palaeontological interest units, as measures of sampling intensity for each period (Fig. 18) . The total number of Cenozoic species was estimated and used to calibrate esti­ mates for earlier geological periods . Each method has its own advantages and dis­ advantages . The empirical, equilibrium, and con­ sensus methods all rely on higher taxa being commensurate and equivalent entities . This is clearly not so (see below) and generic and familial data, though less prone to sampling problems than species data, suffer from other (taxonomic) biases . Bambach' s species richness model does not rely on higher taxonomic diversity but does depend very heavily upon the specific fossil assemblages chosen for analysis (Hoffman 1985) . Only Signor's analysis seems truly to take sampling bias into account, but even this has had to make a number of uncorrobor­ ated assumptions. Species diversity has increased during the Phanerozoic but, because so many biases and prob­ lems beset the estimation of global diversity through time, little else is certain about the precise pattern of this change . Diversity-dependent models of glo­ bal species diversity seem unsupported at present,

447

both on theoretical and empirical grounds (Cracraft 1985; Hoffman 1985) . So long as species-level data primarily reflect the abundance of fossiliferous strata and non-monophyletic data plague taxo­ nomic compilations, assessments of global diversity through time will remain problematic.

Diversity of higher taxa Since the analyses of Simpson (1952) on vertebrate diversity and Valentine (1969) on marine inver­ tebrates, it has been customary to infer evolutionary patterns from the diversity patterns of higher taxo­ nomic catagories such as Order or Family . Both of these authors found that the higher the taxonomic rank analysed the earlier in time was maximum diversity achieved . Taxonomic rank is, however, an arbitrary concept and rank can be given for a number of independent reasons (e . g . to accommo­ date diversity at species level, for paraphyletic 'ancestral' groups, for perceived morphological dis­ tinction, either real, or misconstrued) . Higher taxa appear earlier in the geological record because : (1) the Linnaean system of nomenclature is hierarchical and, as shown by Raup (1983), higher groups must appear earlier in the record than the majority of their subgroups; and (2) traditional taxonomic practice has created paraphyletic higher taxa for dustbin groups comprising primitive early mem­ bers . Higher taxonomic categories are a poor indicator of species diversity if we accept Signor's sampling model (Signor in Valentine 1986) .This is because most higher taxa are currently non-monophyletic the creation of ad hoc classifications . Ranges and durations of higher taxonomic groups are less affec­ ted by sampling bias than species are, but are more affected by taxonomic procedures . Monophyletic groups are real but constitute only a small pro­ portion of currently defined higher taxa . The rest represent groupings made by taxonomists on an arbitrary basis . Clearly, patterns derived from the analysis of largely non-monophyletic data will re­ flect the predelictions of taxonomists and not real biological patterns .

Diversity and extinction Peaks and troughs in diversity through time are sometimes interpreted as evidence for 'adaptive radiation' or 'mass extinction' (Section 2 . 12.3) . How­ ever, rarely is sampling bias adequately taken into account . Taxa can disappear fron, the fossil record

448

5 Taxonomy, Phylogeny, and Biostratigraphy

for three reasons : (1) through biological extinction: (2) through sampling failure; and (3) through taxo­ nomic name change . The first, biological extinction, is obviously what we wish to measure and only monophyletic groups can become extinct biologi­ cally. Paraphyletic groups, unless they include a monophyletic element that survives beyond the first appearance of the derived sister-group, disappear through taxonomist's convention and polyphyletic groups are artificial groupings without reality . Para­ phyletic grades, created when a taxonomist sub­ divides a monophyletic group into two or more subgroups resulting in 'ancestral' groups defined on absence of characters (Section 5 . 2 . 2), generally terminate by pseudoextinction . Sampling failure can to some extent be taken into account through analysis of Lazarus taxa (Section 3 . 12) . If there has been no change in name, Lazarus taxa are easily recognized, but taxonomists may have used gaps in the record as convenient places to divide a plesio­ morphic 'ancestral group' from a derived monophy­ letic portion and only through cladistic analysis can such pseudoextinctions be identified .

References Cracraft, J . 1985 . Biological diversification and its causes. Annals of the Missouri Botanical Gardens 72, 794- 822 . Hoffman, T. 1985 . Island biogeography and palaeobiology: in search for evolutionary equilibria. Biological Reviews 60, 455 -472. Raup, D.M. 1976. Species diversity in the Phanerozoic: a tabulation. Paleobiology 2, 279 - 288. Raup, D.M. 1983 . On the early origins of major biological groups . Paleobiology 9, 107- 1 1 5 . Sheehan, P.M. 1977. Species diversity i n the Phanerozoic: a reflection of labor by systematists? Paleobiology 3, 325 328. Simpson, G . G . 1952. Periodicity in vertebrate evolution. Journal of Paleontology 26, 359 - 370 . Smith, A . B . & Patterson, C. 1988. The influence of taxonomic method on the perception of evolutionary patterns. Evo­ lutionary Biology 23, 127-216. Valentine, J.W. 1969 . Patterns of taxonomic and ecological structure of the shelf benthos during Phanerozoic time . Palaeontology 12, 684 - 709 . Valentine, J.W. (ed .) 1986. Phanerozoic diversity patterns . Princeton University Press and American Association for the Advancement of Science, Princeton.

5.4 Vicariance Biogeography L . GRANDE

Introduction

Biogeography is the study of distribution patterns of animal and plant taxa. It asks the question: 'In what specific geographical area of the Earth does (or did) a given taxon naturally occur?' Vicariance is a name for the process that occurs when a formerly continu­ ous population is divided by the appearance of a barrier . The resulting isolated populations are thought by evolutionists to diverge (speciate) into vicarious taxa taxa that are each other's closest relatives and initially occupy different (non-over­ lapping or allopatric) geographical areas within the original range of the ancestral species. Vicariance biogeography is therefore an historical study that as­ sumes the present geographical distribution of organisms to be the result (at least in part) of an interplay between the biological evolution of taxa -

and the physical evolution of the Earth's surface . It assumes that, if the history of life has paralleled the history of the Earth, then congruent biological and geological patterns of relationships should result. Vicariance biogeography is thought to differ from some more traditional types of biogeographical studies (Section 5 . 5) because it does not look for dispersal (migration over a barrier) of a taxon as an explanation for its current distribution. Vicariance biogeographers do allow that the primitive cosmo­ politanism of an ancestral taxon could have been achieved by enlarging its range through random processes or dispersal (e . g . seeds blown by the wind or carried by migratory birds), but differ from dispersalist biogeographers in their models for causal factors used to explain disjunct distributions and, ultimately, allopatric speciation .

5.4 Vicariance Biogeography Vicariance biogeography has become most popu­ lar during the last 20 years, but it dates back to several monographs by the late phytogeographer Leon Croizat (e . g . 1958, 1964) . State of the art vicari­ ance biogeographical techniques have been dis­ cussed in detail most clearly by Platnick & Nelson (1978), Nelson & Platnick (1980, 1981), Wiley (1981), and Brown & Gibson (1983, pp . 265 271 ) . -

449

ided by a seaway (Fig . 2C), then areas 1 and 2 would have a more recent common ancestry than areas 1 and 3 or-areas 2 and 3 . This geological history indicates that area 1 is more closely related to area 2 than to area 3, independent of any biological evi­ dence (Fig . 2D) . If a biological pattern of area re­ lationships is very strong (repeated many times) vicariance biogeographers would predict that there is probably a general, non-biological (e .g. geological or environmental) explanation .

Methodology The method of vicariance biogeography is to search for general patterns of area relationships based on: (1) the relative relationships of endemic taxa; and (2) historical geology . Such a study might follow four steps: 1 Collect primary data about the relationships within one taxon. For example, we may find that in a family of teleost fishes containing three species (ABCidae in Fig . lA) species A is more closely related to species B than to species C. With at least three taxa in our group we may discover a resolved pattern of relative taxonomic (i . e . phylogenetic) re­ lationships based on a comparative anatomical study .

2 Translate the biological group relationship into a pattern of area relationship. For example (Fig. lA), if

species A is from area 1, B from area 2, and C from area 3, then teleost family ABCidae indicates that area 1 is more closely related to area 2 than to area 3 .

3

Look for a repeating pattern of area relationships .

For example, if plant family XYZaceae is found to have a pattern of phylogenetic relationships as shown in Fig . IB, and species X is from area 1, Y from area 2, and Z from area 3, then plant family XYZaceae indicates that area 1 is more closely related to area 2 than to area 3 and repeats the pattern of area relationships shown independently by teleost family ABCidae . 1f several different groups of organ­ isms indicate the same pattern of area relationships (e . g . Fig . lC), the repeating pattern may reflect some general historical phenomenon . As the strength of the pattern increases, or as the com­ plexity of the repeated pattern increases, the probability of finding congruent patterns of area relationship due to chance alone is diminished.

4 Look for a non-biological (e.g. geological) event which gives the same pattern of area relationships, and is thus a possible causal explanation for the repeating biological pattern . For example, if a large connected area (Fig. 2A) was subdivided by one barrier during Oligocene time (Fig. 2B) and later further subdiv-

Use of fossils in vicariance biogeography Fossils provide additional data which can increase the biogeographical range of a taxon in space or in time (e . g . coelacanths restricted to the western Indian Ocean today were once present in North America and elsewhere; fossil pike [Esocidae] in the Palaeocene indicate that the group dates back to at least 62 Ma) . Fossils also reveal taxa unknown in the Recent biota (e . g . dinosaurs, ichthyodectiform fishes) . Fossil biotas can contribute an additional methodological step that is potentially of use in vicariance studies, and this is time control (Grande 1985) . Vicariance biogeographers generally either use only Recent taxa as data, or a combination of Recent and fossil taxa . If it is accepted that some species disperse, then it must also be accepted that in some areas where sufficient dispersal has occurred, it may be difficult or impossible to recognize a pre­ dominant pattern of area relationships based on the present (Recent) fauna . The predominant area pat­ tern may have been clear at one time but later obscured by conflicting area patterns due to disper­ sal and changing geology (e . g . removal of long­ standing barriers) . For example, a predominant area pattern that reflected some geological event during pre-Eocene time (Fig . 3A) may later have been ob­ scured by a non-congruent pattern (Fig. 3B) super­ imposed during Oligocene time, producing an un­ resolved area pattern in the Recent biota (Fig . 3C) . Fossil biotas, because they are datable, can provide time control, and therefore have the potential to identify area patterns (such as that shown in Fig. 3A) hidden in the Recent biota . By examining only Eocene biotas (assuming Eocene biotas are present in the geographical areas of concern in this example - western North America, western Pacific, and eastern Atlantic), the dispersal event (Fig. 3B) that masked the earlier pattern (Fig. 3A) in the Recent biota can be filtered from the data . If a biota's predominant area relationship pattern changes

5 Taxonomy, Phylogeny, and Biostratigraphy

450 Sp. A (from Area 1 )

Sp· X (from Area 1 )

Area 1

Sp. � (from Area 2 )

Sp. Y ( f r o m A r e a 2)

Area 2

Sp· Z (from Area 3)

Area 3

Sp. � (from Area 3) A

t e leost fam i ly ABCida e

+

B

i n d i cates

Fig. 1 Area cladogram (C) based on biological evidence (A and B).

p l a n t fam i ly XYZ aceae

? -----�� � � ------

---.... ....--.

A

Eocene (one area)

\ Fig. 2

\

2

'f

Area

I � ---�-

� ..7-L

3

-------

� �

Miocene

(mountain range subdivides area)

M iocene

Area

c

B

Oligocene

Oligocene

C

(seaway further subdivides part of area)

Area 1 Area 2

I....---- Area 3

D

Area cladogram (D) based on geological evidence (A, B, and C).

through time from resolved (Fig . 3A) to unresolved (Fig . 3C), then a geological explanation for the disap­ pearance of the pattern (such as removal of a sea­ way, uplifting of a land bridge, or erosion of a mountain range allowing dispersal between pre­ viously isolated areas) can be sought. To identify an area pattern hidden in an area of changing biogeographical affinity, underlying noise (which is due to older incongruent patterns) may also have to be filtered from the data. For example, to identify the predominant Eocene pattern in Fig. 3A, not only must the later Oligocene incongru­ encies be identified but also some older incongru­ encies may need taking into account. Such older incongruencies may be from more ancient groups

of organisms that conformed to much older geologi­ cal and dispersal events . Older data can be filtered out by using only phylogenetically younger groups of organisms (e . g . teleost fishes, rather than gar­ fishes or sturgeons in Fig. 4; see Grande 1985) . The geological history of the Earth has been very dynamic, and through a period of 100 million years, for example, a region's biogeographical affinities might have been affected by several different events . The use of time control on the data can help to sort out the components of a complex (i. e . changing through time) area pattern . Preliminary work (Grande 1985) indicates that time-controlled vicari­ ance studies may be the only practical way to de­ cipher certain complex biogeographical patterns .

5.4 Vicariance Biogeography •

Weste rn N o rt h A m e r i ca Weste rn Pacific co n t i n e ntal reg i o n s

L-___

Easte rn Atl a n t i c conti nental reg i o n s

+

I m m i g ration of seve ral easte r n Atl a n t i c species i nto western N o rt h A m e rica

A

-E

O n ly e n d e m i c b i ota in test a rea n

Weste r n Pacific co n t i n e n t a l regi o n s •

Weste r n N o rt h A m e rica Eastern At l a n t i c co n t i n e ntal regi o n s

c

B

Eocene:

451

Oligocene :

Recent:

D i s pe rs a l eve n t s res u l t i n taxa s h a red b etween weste rn N o rt h A m e rica a n d eastern At l a n t i c

H y b r i d b i ota s h o w i n g n o resolved patte r n of a rea re l at i o n s h i ps (a compos ite pattern of both weste rn Pacific a n d eastern Atl a n t i c aff i n i t i e s fo r western N o rt h A m e r i ca)

Hypothetical model showing how a complex (not strictly vicariant) biogeographical history for a test area (western North America) can result in an unresolved pattern of area relationship in the Recent biota. Descendants of the dispersed taxa of B indicate transatlantic relationships, and obscure the earlier transpacific affinity of the test area . (After Grande 1985 . ) Fig. 3

Teleost f i s h e s

Bowfi n s Ray f i n ned f i s h e s -----I

�----

L-_______

Fig. 4

G a rfi s h e s Stu rgeo n s + Pad d lefi s h e s

Cladogram showing major groups o f actinopterygian

fishes .

Discussion Vicariance biogeography represents an advance in the study of historical biogeography because of its emphasis on rigorous logic and quantitative ana­ lysis rather than using dispersal as an all-purpose explanation for any and all disjunct distributions of organisms . Some studies (Croizat 1958, 1964; Rosen 1975, 1978) have already shown that general patterns of area relationships based on biological organisms exist for discrete areas (i . e . Caribbean land areas) or at higher levels of generality (i . e . world-wide trans­ oceanic) . The full potential of this method is far from realized yet because detailed phylogenetic patterns of interrelationship are still unknown for most groups of organisms . Vicariance biogeogra-

phers hope that once the precise interrelationships of more groups of organisms are understood, the resulting phylogenetic patterns will conform to rela­ tively few general patterns of area relationship . These general patterns could then give evolutionary biologists a fundamental new approach to under­ standing the evolution of the Earth and its biota .

References Brown, J . H . & Gibson, A . C . 1 983. Biogeography. C.V. Mosby Co . , St. Louis, Mo. Croizat, L. 1958. Panbiogeography (3 vols . ) . Published by the author, Caracas. Croizat, L. 1 964. Space, time, form: the biological synthesis . Published by the author, Caracas. Grande, L . 1985. The use of paleontology in systematics and biogeography, and a time control refinement for historical biogeography. Paleobiology 11, 234- 243 . Nelson, G. & Platnick, N . ! . 1980 . A vicariance approach to historical biogeography. BioScience 30, 339- 343 . Nelson, G. & Platnick, N.!. 1981 . Systematics and biogeography: cladistics and vicariance. Columbia University Press, New York. Platnick, N.!. & Nelson G. 1978 . A method of analysis for historical biogeography. Systematic Zoology 27, 1 - 16 . Rosen, D . E . 1975 . A vicariance model o f Caribbean biogeo­ graphy. Systematic Zoology 24, 431 - 464. Rosen, D . E . 1978. Vicariant patterns and historical expla­ nation in biogeography. Systematic Zoology 27, 159 - 188 . Wiley, E . O . 1981 . Phylogenetics: the theory and practice of phylogenetic systematics . Wiley Interscience, New York.

5 . 5 Palaeobiogeography C . R . NEWTON

remarkable concordance between area cladograms for the various taxa indicates a congruence of biogeographical processes, despite differing eco­ logies. Recognition and evaluation of such consistent patterns is a fundamental goal of both biogeography and palaeobiogeography. The central question, as stated by Nelson & Platnick (1981, p. 540) is : 'Might there be a single pattern of relationships (a general cladogram of areas) for all groups of organisms?' This intriguing question may serve as the focus for future cladistic palaeobiogeographical research. Few cladistic palaeobiogeographical studies have thus far been conducted, largely because of con­ straints on databases suitable for cladistic analysis . Firstly, the prerequisite o f rigorous phylogenetic cladograms severely limits the number of fossil groups and areas that can be analysed using cladistic biogeography Gablonski et al. 1985) . Secondly,

Introduction Palaeobiogeography is the study of the spatial distri­ bution of ancient organisms, including analysis of the ecological and historical factors governing this distribution. Just as there is considerable overlap between the fields of ecology and biogeography, so there also exists a scientific continuum between certain aspects of palaeoecology and palaeobiogeo­ graphy. Most palaeobiogeographical studies have dealt with distributions of individual taxa or with questions of global or regional provincialism. Under the rubric 'palaeobiogeography' are two disparate subfields differing more in objectives than in methodology. Applied palaeobiogeography, repre­ senting the larger body of work, seeks to use the distribution of fossils as a tool for solving palaeogeo­ graphical, palaeoclimatological, or tectonic prob­ lems. In contrast, palaeobiogeography in the strict sense addresses the 'why and how' of the distri­ bution of ancient organisms, including environ­ mental, biological, and historical controls on habitable area (see also Section 5.4) . Curiously enough, this second area of inquiry has been less explored, possibly because of the difficulty in de­ ciphering process from pattern, with such a large number of variables and an admittedly imperfect fossil record (Section 3 . 12) .

A

�

A u stral i a Au stral i a N ew G u i nea N ew G u i nea S o u t h A m e r i ca S o u t h A m e r i ca �--- N o rth A m e r i ca

E u rope

Methods in palaeobiogeography

D

B

A u stral i a

A u s t ra l i a

Two competing schools have each developed meth­ odologies to document and compare biogeographi­ cal and palaeobiogeographical patterns . Cladistic biogeography, which has borrowed heavily from the field of cladistic systematics (Section 5 . 2 . 2), uses area cladograms to consider the geographical re­ lationships of species from monophyletic groups . The basic premise o f this technique i s that areas, like taxa, can be arranged in hierarchical groups that define levels of affinity between geographical regions . The most rigorous examples of cladistic biogeography have been based on taxonomic groups for which phylogenetic cladograms are also available . For example, Fig . 1 compares area clado­ grams for a variety of different animal taxa. The

N ew G u i nea N ew G u i nea South A m e rica S o u t h A m e r i ca N o rt h A m e r i ca E u rope E u rope

Biogeographical area cladograms . A, For osteoglos­ sine fishes and chelid turtles. B, For ratite birds . C, For galli­ form birds. D, For hylid frogs. Note the concordance of area cladograms for these groups of modern organisms. (From Patterson in G. Nelson & D . E . Rosen (eds) Biogeography: a critique. Copyright © 1981 Columbia University Press. Used by permission.

Fig. 1

452

453

5.5 Palaeobiogeography

phylogenetic relationships to aid in pattern inter­ pretation, neither monophyly nor prior evolutionary studies are absolute prerequisites for phenetic bio­ geographical analysis . A second and more practical difference is that phenetic analysis is not confined to pattern analysis of endemic taxa, but can readily accommodate widespread species or species whose ranges include more than one area. This latter prop­ erty makes phenetic methods simpler to apply for groups with complex, overlapping distribution pat­ terns (e . g . Indo-Pacific molluscs) . Numerous similarity coefficients have been ap­ plied to phenetic biogeographical analysis, as well as to phenetic palaeobiogeographical analysis . Each of these numerical indices has idiosyncratic proper­ ties that affect biogeographical and palaeobiogeo­ graphical results (see Table 1, for some of the more

cladistic area analysis is relevant primarily for en­ demic taxa whose phylogenetic interrelationships are known; more widespread taxa or overlapping taxa occupying several regions are accommodated only with difficulty in the cladistic approach . This second restriction is at least as great as the first, because these latter groups constitute by far the majority of species (modern and ancient) . The competing school of phenetic biogeography emphasizes use of similarity coefficients or other quantitative techniques as applied to whole-fauna comparisons . This approach was pioneered by palaeontologist G . G . Simpson, in an attempt to quantify similarities between modern faunas . Two aspects of phenetics provide striking contrast with the cladistic biogeographical method . Firstly, al­ though some phenetic biogeographers do use

Table

1 Properties of selected similarity indices used in palaeoecology and palaeobiogeography. 1

2

Coefficient

As C � O

C N1 + N2 - C C+A . . SImple matchings NI + N2 - C + A C S0renson N1 + N2

C 2El + C

1 Jaccard

�

---

2

�

-----

3

.

4 1 st Kulczynski

C N1 + N2 - 2 C

�O

C2 N1 N2

7

Correlation ratio

8

Slmpson ­

9

Braun -Blanquet ­

C NI

C N2

1 C VN1 N2 2y'l\!;

10 Fager ---

--

NI N2

-

1 = - and

2

1 6

�O

� 1

�O

�

�O

� 1

3 8

-

�O

� 1

VS

-

-> 0

-> 1

1 8

-> 0

-> 1

2

� O

-> 1

4

-

1 = Simpson (8) - __

2N1

J

->

2

1

- 2y'l\!;

1 =-

2

[if A

=

C

'

then =

! 3

J

4

00

� 1 -

C NI

-

1

5

� 1

C+A 5C + A

C . [= Slmpson (8)] NI C . � [= Slmpson (8)] N1 C2 � -2 [= (Simpson (8» 2 ] ( NI ) C NI C . � [ = Slmpson (8)] NI 1 C � NI - 2�

[

If

C+A 2E 1 + C + A

�

.

4

3

1

1

1

1

2y'l\!; VS 1

--

1

4VC 1

C number of species common to both samples; E1 species present in less diverse sample; E2 = species present in more diverse sample; A species absent; N1 = total number of species present in less diverse sample; N2 = total number of species present in more diverse sample . (After Valentine 1973 . ) =

=

=

454

5 Taxonomy, Phylogeny, and Biostratigraphy

commonly used similarity coefficients in phenetic analysis) . The Simpson similarity coefficient, for example, is relatively insensitive to disparities in sample size and sampling intensity compared with the Sorenson coefficient, in which both NI and N2 (species richnesses of two sites or areas) contribute information . It is not always a straightforward matter to compare results from different types of similarity comparisons . Some degree of standardi­ zation is, however, afforded by the widespread use of the Sorenson, Simpson, and Jaccard coefficients in both biogeographical and palaeobiogeographical studies . A variety of clustering techniques can be applied to the resulting similarity matrices (Fig. 2) in order to simplify relations between sites or areas, where the patterns are too complex to resolve by simple inspection (unfortunately, this is frequently the case) . One substantial contribution to the phenetic bio­ geographical school has been the proposal of new similarity indices whose probability distributions are known. A serious flaw in the Sorenson, Simpson, and Jaccard coefficients had been that their probability distributions were unknown and testing for significance of differences between vari­ ous elements of the matrices was not possible . Alter­ native similarity indices with known probability distributions have been proposed independently by several different investigators (see review in Jablonski et al. 1985) . The revised methodologies proposed by these workers have thus provided a means of rigorous statistical testing of biogeo­ graphical classifications, and have further provided a way of weighting biogeographical data to compen­ sate for the overemphasis of widespread taxa that had formerly been typical of phenetic similarity comparisons . Palaeobiogeographers have traditionally adopted phenetic rather than cladistic approaches to the recognition and comparison of ancient provinces . One reason for this i s that the comparability of modem and ancient provinces using phenetic methods has been well established. This preference also stems from the restrictive prerequisites for cladistic analysis .

Palaeobiogeographical inference and interpretation Recent challenges to the validity of the ad hoc expla­ nations common in palaeobiogeography have brought about attempts to formalize procedures for

ALEUTIAN

. 47

. 37

OREGON I A N

. 28 . 19

. 42

. 70

SURIAN

. 16

. 31

. 53

. 72

. 10

. 22

. 44

. 50 . 57

CALIFORNIAN

PANAMANIAN

. 58

. 21

. 52

.13

. 36 . 70

. 09

. 24

. 49

. 66

. 04

.14

. 27

. 37

. 48

Gastropods

Bivclves Jaccard's Coefficient

ALEUTIAN

.97

OREGONIAN

. 94

CALIFORNIAN SURIAN PANAMANIAN

.78

. 89

. 81

.63 . 68 . 56

. 87

. 60

.97

. 65

. 71 .75

.88 .79

Bivalves

.91

. 89

.65

.79

.93

.45

. 59

.74

. 37

. 59

.79

.72 .78

.94

Gastropods

Simpsan's Coefficient

Fig. 2 Similarity matrices for bivalve and gastropod genera in different modern molluscan provinces, calculated using the Jaccard and Simpson coefficients . (From Campbell & Valentine 1977.)

biogeographical and palaeobiogeographical infer­ ence and interpretation . At issue are the largely anecdotal 'narrative explanations' traditionally used in these fields (Ball 1976) . Critics have charged that the strictly inductive procedures and excessive reliance on Occam's razor have encouraged expla­ nations which, though rational, are unique to indi­ vidual case studies and hence have no predictive power (Ball 1976) . Alternatives to the ad hoc mode of explanation have been put forth by proponents of both vicariance and dispersal biogeography. Vicariance biogeography (Section 5 . 4) emphasizes the role of tectonic and other environmental pro­ cesses in forming barriers that, in turn, cause geographical isolation and promote allopatric speciation. Proponents of vicariance biogeography have pointed out that a vicariant hypothesis can often be falsified by geological evidence; in contrast, claims for sweepstake and other chance dispersal are often not falsifiable (Platnick & Nelson 1978) . The vicariant procedure of palaeobiogeographical or biogeographical hypothesis-testing proceeds first through a test for vicariant processes and then on to other explanations if vicariance is not sufficient or

455

5. 5 Palaeobiogeography is inconsistent with geological evidence . The struc­ ture of vicariant biogeographical analysis demands consideration of a minimum of three taxa and three geographical areas, so that two-taxa or two-area problems cannot be solved using this approach . Classic examples of vicariance events include clos­ ure of the Panamanian isthmus, separation of the major components of Pangaea, and opening of the Atlantic Ocean . However, tectonic events are not the only controls on biogeographical patterns . Dispersal biogeography, an alternative mode of interpretation, stresses mo­ tility and reproductive strategies as primary controls on distribution patterns . Dispersalist interpret­ ations can be found in case studies using both cladistic and phenetic methodologies for biogeo­ graphical pattern analysis, so that there is no simple link between method and interpretative mode . De­ spite charges by vicariists that dispersalist hypoth­ eses cannot be falsified, in fact recent developments in palaeobiology have greatly strengthened the capabilities for testing dispersal hypotheses in palaeobiogeography. Foremost among these developments are break­ throughs in interpreting larval strategies of fossil invertebrates . For molluscs, protoconch and prodis­ soconch morphology of gastropods and bivalves can often be used to differentiate planktotrophic (plankton-feeding) from non-planktotrophic veliger larval forms . Although this dichotomy does not exactly coincide with dispersal capability (for some

planktotrophic species have short residence times in the plankton and one lecithotrophic echinoderm does not settle for 30 days; Jablonski & Lutz 1980), in general planktotrophs are able to disperse more widely than non-planktotrophs . Some planktic larvae certainly disperse very widely as a conse­ quence of oceanic gyres (Fig. 3) . Geographical range and species longevity of fossil invertebrate s correlate very well with inferred repro­ ductive strategy, at least in some case studies . Studies of larval types in Cretaceous and Tertiary gastropod species of the Gulf of Mexico (Hansen 1980; Jablonski 1982) clearly indicate that non­ planktotrophs had shorter durations than their planktotrophic counterparts (among Tertiary neo­ gastropods, one million years versus five million years, respectively; Hansen 1980) (Fig . 4) . Plankto­ trophy also correlates well with expanded geo­ graphical range of fossil gastropods; Jablonski (1982) found that among Cretaceous Gulf gastropods planktotrophs had median ranges of 1600 km, as compared with only 250 km for non-planktotrophs . Thus, identification of larval types may enable dis­ persalist models to be tested rigorously, particularly in those cases where closely related modern groups contain both planktotrophic and lecithotrophic representatives for morphological comparison . Not all palaeobiogeographical dispersal hypo­ theses can be tested adequately. Perhaps the most difficult case to evaluate in the fossil record is the claim that the 'sweepstakes' or 'jump' modes of

Fig. 3 Occurrence of veliger larvae of the gastropod family Architectonidae in plankton tows in the tropical Atlantic Ocean, Philippia krebsii; triangles Architectonica nobilis; open with directions of surface currents indicated by arrows. Filled cV-des site s where architectonids were absent. (From Scheltema in Gray & Boucot 1979 .) cirdes other architectonids; smallest dots =

=

=

=

5 Taxonomy, Phylogeny, and Biostratigraphy

456

dispersal have played an integral role in the distri­ bution of ancient organisms . These two dispersal modes both involve infrequent events and very small numbers of individuals that colonize sites far from the site of the parent population. Given the enormity of geological time, such improbable events have doubtless occurred . However, a palaeobiogeo­ graphical hypothesis that relies exclusively on this process is not particularly informative and cannot be falsified (Ball 1976; Platnick & Nelson 1978) .

locomotion (see discussion above concerning plank­ totrophs vs . non-planktotrophs in Cretaceous and Tertiary Gulf Coast faunas) . Hollow curves are also known for palaeobiogeo­ graphical area distibutions . Fig . 4, from Hansen's (1980) work on Tertiary neogastropods, shows hollow curves for both planktotrophic and non­ planktotrophic species, although the steeply nega­ tive slope characteristic of most hollow curves is far better developed among non-plallktotrophs .

Biogeographical and palaeobiogeographical area distri­ butions. A central issue in palaeobiogeography is

Latitudinal

and

longitudinal

diversity gradients.

Among the many biogeographical distributions known for modern organisms, two truly first-order patterns emerge . These are a pervasive latitudinal diversity gradient, in which most groups have maxi­ mum species diversities at low latitudes and de­ creasing diversity in temperate and polar regions; and a marine longitudinal diversity gradient, in which many taxa have highest diversities in the Indo­ west Pacific region, with diminishing diversity away from this species-rich area. The origin and geological history of these present-day biogeo­ graphical patterns have inspired much debate . Of particular importance to palaeobiogeography is the question of whether these first-order patterns have persisted throughout Phanerozoic time or, alter­ natively, have arisen in response to late Cenozoic events and configurations . The latitudinal gradient in marine and terrestrial

the relation between biogeographical distribution and evolutionary rates in the fossil record. Flessa & Thomas (1985) have shown that biogeographical area distributions may yield 'hollow curves' . These distri­ butions reflect the occurrence of taxa in one or more regions . As an example, Fig. 5 illustrates that most modern marine bivalve genera exist only in a few regions, whereas a few genera are extremely wide­ spread . Modelling of biogeographical areas to pro­ duce this hollow curve suggests that the probability of geographical range expansion must increase with increasing geographical range; as Flessa & Thomas (1985, p. 367) commented, 'Like the rich getting richer, the cosmopolitans become more cosmopoli­ tan' . The disparity between endemic and cosmopoli­ tan taxa relates in some (but certainly not all) cases to contrasting reproductive strategies or modes of

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diversity apparently has persisted throughout much, if not all, of Phanerozoic time . It has been recognized in many palaeobiogeographical ana­ lyses, including studies on Cretaceous foraminifera (Fig. 6) . One possible cause, the 'diversity-pump' hypothesis (Valentine 1984), involves extermination of high-latitude representatives of species during cooling events, leading to accumulation of higher diversities in lower-latitude portions of species' ranges . A further, special case of this temperature­ mediated diversity model is the scenario of con­ comitant warming of the tropics and cooling of the poles, in which additional niches might be opened up at the boundary between tropical and subtropical zones; this mechanism is especially applicable to the last 20 million years (Valentine 1984) . A third possible influence on the origin of the latitudinal diversity gradient is the long-term environmental stability of the tropics vs . the seasonal instability of temperate and polar regions . The origin and geological longevity of the high­ diversity region in the Indo-west Pacific and declin­ ing diversities away from this region are even more controversial. Some workers have linked the high Indo-west Pacific diversities with the overall warm, equable temperatures of the region and have associ­ ated the peripheral diversity declines with lowered sea-surface temperatures . Another option, the vicariance-and-refuge model, stresses the physio­ graphical dissection of the region and the presence of multiple, active tectonic blocks that have pro­ duced vicariant divergence within small, active­ margin basins (Rosen 1984) . If this latter model proves correct, then the Indo-west Pacific diversity high and longitudinal diversity gradient may well be an artifact of Cenozoic tectonic configurations .

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Pacific basin palaeobiogeography. Most palaeobiogeo­ graphical research (including the case studies cited above) emphasizes distribution patterns of organ­ isms on continents or continental margins, particu­ larly the major components of Pangaea . However, biogeographers have long been aware of the impor­ tance of islands in biogeographical distribution pat­ terns . A.R. Wall ace, for example, understood that islands often provide remarkable case studies for analysis of distributions and dispersal, and that the diversity and composition of island faunas depend greatly on the geological history of the island . Several controversial studies of Pacific biotas have prompted a re-evaluation of the role of island faunas and floras in palaeobiogeography . Contrary to the prevailing notion that West Tethys was the pre­ dominant centre-of-origin for shallow-marine diversity during Mesozoic time, Kristan-Tollman & Tollman (1982 and subsequent papers) have suggested that oceanic islands provided 'stepping­ stone' dispersal from the Americans westward to Europe . Tozer (1982) also reconstructed Triassic ammonoid biogeography using a model of tectono­ stratigraphic terranes as islands widely dispersed in the Panthalassic (ancient Pacific) ocean . The mixed biogeographical affinities of some of these circum-Pacific terranes resemble the mosaic biogeo­ graphical patterns found in modern oceanic islands such as the Hawaiian chain (Newton 1987) . Applied palaeobiogeography. In some cases, palaeo­ biogeographical data can be used to resolve

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geological problems, particularly those of a palaeo­ climatic or tectonic nature (see also Section 5 . 1 1 ) . For instance, the highly anomalous palaeobiogeo­ graphical patterns of fusulinaceans in the western Cordillera of North America provided the initial impetus for the concept of exotic or 'suspect' tecto­ no strati graphic terranes on the North Pacific rim (Fig . 7) . Work on Jurassic ammonites has also sug­ gested dramatic northward translation of many Cordilleran tectonostratigraphic terranes (Tipper 1981) . These Jurassic studies are particularly note­ worthy in that cratonal latitudinal zonations had

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been well established for the ammonoids, so that Cordilleran tectonic displacement could be esti­ mated. A very useful summary of Pacific faunal anomalies related to terrane displacements has been presented by Hallam (1986) . In addition to work in the Pacific basin, applied palaeobiogeographical studies have contributed to tectonic models of separ­ ation of the Gondwana continents, and have also served as tests of pre-existing tectonic models in the complex Caribbean region . As valuable as some of these studies have been, fauna-based palaeogeographical reconstructions

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460

5 Taxonomy, Phylogeny, and Biostratigraphy

have sometimes been spectacular failures . Patterns of disjunct endemism, unevenness of sampling, and lack of adequate systematics have often led to er­ roneous interpretations or fruitless arguments . Be­ cause of these inherent shortcomings, fossil data without supplemental geological data cannot yield reliable tectonic reconstructions . None the less, with adequate sampling, an excellent systematic base, and an ecologically diverse group of fossils, some fruitful comparisons between expected and observed palaeobiogeographical distributions may be made (Newton 1987, 1988) . One real advantage is that, despite other flaws, the palaeogeographical models that result from applied palaeobiogeography are usually testable, even if not always correct .

Palaeobiogeography and extinction. One of the most exciting and promising aspects of palaeobiogeo­ graphy concerns the relationship between biogeo­ graphical area and extinction. Jablonski (1986) has shown that wide geographical range typically con­ fers longer species longevities during 'background' intervals, but does not correlate well with longer lineage durations during mass extinctions (Fig. 8) . This is similar to ecological traits such as larval planktotrophy, which, as discussed above, corre­ lates well with species durations during steady­ state or 'background' intervals but not during mass extinctions . The positive correlation between large geographi­ cal range and minimal losses during mass extinctions also obtains at higher taxonomic levels . For example, Hallam (1981) showed that for Triassic bivalves, losses during the end-Triassic marine mass extinc­ tion were greater for those genera that were endemic (in this case, found in three or fewer regions) and lesser for those that were cosmopolitan (found in more than three regions) . Further investigation of this intriguing link between palaeobiogeography and extinction may reveal much about the origin of mass extinctions (see also Section 2 . 12) .

References Ball, 1.R. 1976 . Nature and formulation of biogeographical hypotheses. Systematic Zoology 24, 407-430 . Campbell, CA. & Valentine, J.W. 1977. Comparability of modern and ancient marine provinces . Paleobiology 3, 49- 57. Flessa, K.W. & Thomas, R.H. 1985 . Modelling the biogeo­ graphic regulation of evolutionary rates. In: J. W. Valentine (ed . ) Phanerozoic diversity patterns: profiles in macro­ evolution, pp . 355 - 376. Princeton University Press, Princeton, N.J. Gray, J . & Boucot, A.J. (eds) 1979 . Historical biogeography: plate tectonics and the changing environment. Oregon State

University Press, Corvallis, Or. Hallam, A. 1981 . The end-Triassic extinction event. Palaeogeo­ graphy, Palaeoclimatology, Palaeoecology 35, 1 -44. Hallam, A. 1986. Evidence of displaced terranes from Penman to Jurassic faunas around the Pacific margins . Journal of the Geological Society of London 143, 209 -216. Hansen, T.A. 1980. Influence of larval dispersal and geo­ graphic distribution on species longevity in neogastro­ pods . Paleobiology 6, 193-207. Jablonski, D . 1982 . Evolutionary rates and modes in Late Cretaceous gastropods: role of larval ecology. North American Paleontological Convention Proceedings 1, 257-262. Jablonski, D. 1986. Background and mass extinctions : the alternation of macroevolutionary regimes. Science 231, 129- 133. Jablonski, D. & Lutz, R.A. 1980. MolIuscan larval shell morphology: ecological and pale ontological applications. In: D.C Rhoads & R.A. Lutz (eds) Skeletal growth of aquatic organisms, pp . 323- 377. Plenum, New York. Jablonski, D . , Flessa, K.W. & Valentine, J.W. 1985 . Biogeo­ graphy and paleobiology. Paleobiology 11, 75 -90. Kristan-Tollman, E . & TolIman, A. 1982 . Die Entwicklung der Tethystrias und Herkunft ihrer Fauna. Geologische Rundschau 71, 987-1019. Monger, J.W.H. & Ross, C A . 1971 . Distribution of fusi­ linaceans in the western Canadian CordiIlera. Canadian Journal of Earth Sciences 8, 262. Nelson, G . & Platnick, N . 1 . 1981 Systematics and biogeography: cladistics and vicariance. Columbia University Press, New York. Newton, C R . 1987. Biogeographic complexity in Triassic bivalves of the Wallowa terrane, northwestern United States: oceanic islands, not continents, provide the best analogues . Geology 15, 1126 - 1 129. Newton, CR. 1988 . Significance of 'Tethyan' fossils in the American CordiIlera. Science 242, 385 - 391 . Patterson, C 1981 . Methods of palaeobiogeography. In: G . Nelson & D . E . Rosen (eds) Biogeography: a critique, p . 482. Columbia University Press, New York. Platnick, N.1. & Nelson, G. 1978. A method of analysis for historical biogeography. Systematic Zoology 2 7, 1 - 16 . Rosen, B.R. 1984. Reef coral biogeography and climate during the Cainozoic: just islands in the sun or a critical pattern of islands? In: P.J. Brenchley (ed . ) Fossils and climate, pp. 201 -262 . John Wiley, New York. Stehli, F . G . , Douglas, R . G . & NewelI, N . D . 1969 . Generation and maintenance of gradients in taxonomic diversity. Science 164, 947-949 . Tipper H.W. 1981 . Offset of an upper Pliensbachian geo­ graphic zonation in the North American CordilIera by transcurrent movement. Canadian Journal of Earth Sciences 18, 1788 - 1 792. Tozer, E.T. 1982 . Marine Triassic faunas of North America: their significance for assessing plate and terrane move­ ments . Geologische Rundschau 71, 1077- 1 1 04. Valentine, J.W. 1973 . Evolutionary paleoecology of the marine biosphere. Prentice-HalI, Englewood Cliffs, N.J. Valentine, J.W. 1984. Neogene marine climate trends : impli­ cations for biogeography and evolution of the shallow-sea biota . Geology 12, 647-650.

5 . 6 Biostratigraphic Units and the Stratotype/Golden Spike Concept C . H . H O L L AND

Biostratigraphy

assemblage of fossils, of which one abundant and characteristic form is chosen as an index . Apart from the more generally applicable term biozone, there is really a whole family of qualified biozonal terms . The development of some of these and the attendant notions of equivalent time were clearly charted by Arkell (1933) . The kinds of biozone now usually recognized include the assemblage bio­ zone, acme biozone, total-range biozone, local­ range biozone, concurrent-range biozone, and consecutive-range biozone (Section 5 . 7) . Biozones continue to be used with great success and consist­ ent correlation is achieved thereby. Yet some workers comment that their definition is often imprecise . The ultimate defence must be that the method does in practice work and the whole edifice of stratigraphy is really built upon it. It is important that those employing biozones define the units they are using. Certain groups of fossils, notably the trilobites in the Cambrian, the graptolites in the Ordovician and Silurian, and the ammonites in the Mesozoic, have been used with such success that German strati­ graphers, in particular, have been inclined to think of a primary orthostratigraphy based upon such a group and subsidiary parastratigraphy employing other fossils . In many circumstances, of course, such forms are not readily available and it is more impor­ tant than ever to refer to whole faunas or floras . Perhaps the most striking development in more recent years has been the increasing importance of micropalaeontology in biostratigraphy, going far beyond the long established use of foraminiferans in Tertiary studies to the widespread employment of acritarchs, spores, chitinozoans, conodonts, and ostracodes . With macrofossils it is possible for the experienced worker to make some attempt at cor­ relation even before laboratory examination can be undertaken. With microfossils, where initial preparation is required, this unfortunately is not possible . For most stratigraphers across the world bio­ stratigraphy does not stand alone as the only kind

Biostratigraphy is the use of fossils in stratigraphic correlation . In stratigraphy, correlation is the heart of the matter . By its means local stratigraphic successions and the interpretations of these as se­ quences of events in geological history can be brought together in a regional or world-wide pic­ ture . In the Archaean and in the earlier part of the Proterozoic, where fossils are very rare, radiometric dating and such other features as structural episodes may provide the only available means of correlation. In contrast, in the very youngest rocks a whole variety of stratigraphic tools, including magneto­ stratigraphy and the study of climatic changes, may be brought to bear. In the Late Proterozic and in most of the Phanerozoic, biostratigraphy provides often the only and almost always the most accurate method of correlation . In the Silurian, for example, biostratigraphic units with individual time ranges of only about one million years are available (Hol­ land 1986) . In the Mesozoic even greater precision is easily achieved . Such resolution is unobtainable from radiometric dating, useful though this may be in giving indications of placing in time and of the rates of processes. Biostratigraphy has its origin in the pioneering work of W. Smith in the early part of the nineteenth century . As his land surveying took him farther afield from his base in Somerset in southwest England, Smith began to realize that, even though he might no longer use lithological characteristics to recognize his position in the stratigraphic suc­ cession, the contained fossils could be relied upon as indices . Thus was established one of the great principles of stratigraphy: that strata may be recog­ nized by their 'organized fossils' . Smith was a practical man and it was only through later, more philosophical approaches that there came develop­ ments such as Oppel' s use of zones (Hancock 1977) . A general definition of the most frequently used kind of zone (which is better now always referred to as a biozone in contradistinction to the chronozone) is that it is a belt of strata characterized by an

461

462

5 Taxonomy, Phylogeny, and Biostratigraphy

of stratigraphy. Most would now recognize litho­ stratigraphy as another category . The formation is the fundamental unit in lithostratigraphy and this is e ssentially a mappable unit based upon the litho­ logy of the rocks included within it. The necessity for such units became most apparent in situations where primary geological mapping was being undertaken in modern terms and often in difficult terrain; where the necessity to produce the geo­ logical map, which was likely to be of economic importance, left no possibility or no time for the niceties of palaeontology . There has been sub­ sequent discussion as to the extent to which fossils may sometimes play a part in the recognition of litho­ stratigraphic units. Holland (1978) put the matter as follows . 'In fact the grey area between the black and white of lithostratigraphy and biostratigraphy may well be small . Biozones based, for instance, upon trilobites, graptolites, or ammonites will usually be readily distinguishable from fossiliferous forma­ tions . Groping towards a diagnosis in words, it seems that there is a kind of mathematical property of biozones involving sets or sequences' . Or, as Holland et al. (1978) put it: 'The use of fossils in lithostratigraphy is clear in those cases where they form part of the grossly recognisable lithology of the rock: as in coral beds, coquinas, plant beds, etc. There is, however, a less clear area closer to bio­ stratigraphy, where lithostratigraphic units are de­ fined, partly at least, by the identification of fossils . As such these units must remain readily recognis­ able and, in general, mappable . '

Global standard stratigraphy
These boundaries are time-surfaces ' How, it may reasonably be asked, can one recognize a strati­ graphic unit whose boundaries are independent of physical characters? The Stratigraphy Committee of the Geological Society of London pointed the way to the practice which is now being followed by the component bodies of the Commission on Stratigraphy of the International Union of Geological Sciences (Section 5 . 8) in establishing that chronostratigraphic units must be defined on the basis of internationally agreed boundary stratotype sections (Section 5 . 10) . The base of each division is defined by a point in the section and this point has become known as the golden spike. The unique property of the golden spike (Fig. 1) is that here and here alone a defined point in rock is known (by definition) to coincide with a defined point in time . This reference point defines the base of the chronostratigraphic or glo­ bal standard division in question . Its top is defined by the base of the division above . From the bound­ ary stratotype the boundary is extended as accu­ rately as possible using all available methods of correlation. These will usually be biostratigraphic. The important point is that, though the boundary so extended geographically through rock may ap­ proximate to equivalence with a boundary in time, it will probably never be known how closely this ideal is achieved . It is only at the golden spike that we can, by definition, be sure . Fig. 1 shows the way that a particular biostratigraphic unit may be used to carry a boundary in correlation . A flagrantly diachronous lithostratigraphic unit is added to the figure for completeness. The term global standard stratigraphy is preferred to chronostratigraphy, both for its emphasis upon a unique internationally agreed standard and because it removes to some extent the unfortunate con­ notation with time . We (hypothetically) hammer golden spikes into rock, not into time . Parastrato­ type sections may be useful in some large regions or where the facies of the division is very different. These must be correlated as closely as possible with the standard stratotype and the latter must always have precedence in determining diagnosis . Regional chronostratigraphic divisions may be employe d where, at the lower levels of the hierarchy, cor­ relation is not possible with the stratotype for the global standard division in question. Their con­ tinued use in the wide territories of the U . S . 5 .R. is obviously thought to be helpful, particularly in the case of the regional stage or gorizont (Holland 1983) . It is to be hoped that all such regional divisions will .

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5 . 6 Biostratigraphic Units and Golden Spike Concept

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gradually disappear as correlation with the global standard becomes more and more comprehensive and more and more precise . Disregarding the bemusing notion that global standard divisions are defined by time planes, there is a more serious problem affecting the widespread acceptance of global standard or chronostratigraphic units and the idea of the golden spike as employed in their definition . It springs from the history of stratigraphy as it has been practised in highly fossi­ liferous, ammonite rich Mesozoic rocks (Hancock 1977; Holland 1986) . Mesozoic stratigraphers have found it convenient to group their biozones into stages . Arkell (1956a), the doyen of Jurassic stratigraphers, saw the advan­ tage of this as 'allowing several zones to be corre­ lated in a general way over long distances when the zones individually are too precise' . Thus the stage in particular has become a contentious division in stratigraphy, some workers regarding it as that level in the global standard or chronostratigraphic hier­ archy which comes below the series, others seeing it simply as a biostratigraphic unit involving the grouping of biozones . Mesozoic stratigraphers do appear to accept the necessity for internationally agreed schemes of biozones and stages and the necessity for internationally agreed stratigraphic divisions of a higher category, such as the system . Their sequence of ammonite biozones is now more or less standardized and, even if they cannot see their way to giving geographical names for these, they can provide boundary stratotypes for them . Thus their biozones would become chronozones, neatly falling into place in a global standard strati­ graphy leading down from the system and then series, to the stage and then chronozone . In the

Palaeozoic there is as yet much less standarization of biozones, though Koren (1984) has pointed the way in her preliminary treatment of Silurian grap­ tolite biozones . These may eventually become chronozones and thus take their place in a global standard hierarchy which is already becoming es­ tablished by international agreement at higher levels . Fig. 2, for example, shows the agreed scheme for the Wenlock Series within the Silurian System (Bassett et al. 1975) . This is the one place where two chronozones have already been properly defined, though the international machinery of standardi­ zation is not yet operating at this high level of resolution . The Whitwell Chronozone, its base defined at a boundary stratotype in the Welsh borderland, corresponds in range there to that of the Cyrtograptus lundgreni Biozone, one of very widespread recognition . The succeeding Gleedon Chronozone is similarly defined at a stratotype, but there comprises the ranges of both the Gothograptus nassa and Monograptus ludensis Biozones . These two chronozones make up the Homerian Stage, the upper of the two stages into which the Wenlock Series is now divided . It has not been adequately recognized that such a hierarchy of divisions is needed in order to express different degrees of precision in stratigraphy . Fig. 3 summarizes the common procedures in stratigraphic classification within the Phanerozoic. With few exceptions it is only at the golden spike that there can be direct connection between litho­ stratigraphy and the global standard scheme . Usually, correlation will be achieved through biostrati­ graphy, as indicated by the thick arrow on the diagram . The additional time terms such as period and era are necessary only for purposes of language .

464

5 Taxonomy, Phylogeny, and Biostratigraphy

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5. 6 Biostratigraphic Units and Golden Spike Concept Thus one cannot speak of dinosaurs living in the Jurassic System, but rather that they lived in the Jurassic Period. Geochronometry achieved through radiometric dating is a different matter, though a connection between this and biostratigraphy is indicated on the figure as biochronology . The term biochronology is appropriate in those as yet rare cases in which a most detailed event stratigraphy allows the precise coupling of radiometric dates with biostratigraphy. E . G . Kaufmann and his colleagues have achieved this in the Western Interior Basin of North America, where within the Cretaceous some 400 bentonites or other volcanic related layers provide a succession of isochronous surfaces which have been dated by the potassium- argon method to give a resolution of fractions of a million years . This chronology is linked with a most detailed ammonite and bivalve biostratigraphy. Such fine tuning is unlikely to be frequently achieved, even at this particular level, and thus it remains important that an internationally agreed global standard stratigraphy is maintained .

Concluding comments In summary, biostratigraphic units are bodies of strata characterized by their fossil content. As Arkell (1956b) put it: 'without the fauna a zone is nothing: a will-o'-the-wisp, without substance, unrecognis­ able' . Global standard stratigraphic divisions (chrono­ stratigraphic divisions) are bodies of strata re­ presenting divisions of the internationally agreed hierarchy including era, system, series, stage, and chronozone . Their definition depends upon selected marker points (golden spikes) in basal boundary stratotype sections (Section 5 . 10), the choice having been ratified by the International Union of Geologi­ cal Sciences (lUGS) acting through its Commission on Stratigraphy (Section 5.8) . In few cases as yet have international procedures achieved completion . The Subcommission on Silurian Stratigraphy has a fully agreed scheme and in some other systems, such as the Devonian, matters are well advanced . In the meantime the names for the various systems are generally accepted. It is important that once the horizons for boundaries between global standard

465

divisions are chosen, and once the golden spikes in boundary stratotype sections are agreed and the whole matter ratified by the International Union of Geological Sciences, these decisions are ac­ cepted for the reasonable future, so that stability is assured and fundamental work can move ahead against a rational and clear background . It is impor­ tant to recognize that no boundary stratotype is likely to be perfect in all respects . It is too much to expect that sections will be found which have all the desirable attributes. It is also important to recognize that there is some urgency about the matter and, above all, that nationalism has no place in strati­ graphy.

References Arkell, W.}. 1933. The Jurassic System in Great Britain . Oxford University Press, Oxford. Arkell, W.}. 1956a. Jurassic geology of the world. Oliver and Boyd, Edinburgh. Arkell, W.}. 1956b. Comments on stratigraphic procedure and terminology. American Journal of Science 254, 457467. Bassett, M . G . , Cocks, L . R . M . , Holland, C . H . , Rickards, R.B. & Warren, P.T. 1975 . The type Wenlock Series. Report of the

Institute of Geological Sciences

75/13 .

Hancock, } . M . 1977. The historic development of concepts of biostratigraphic correlation . In: E . G . Kaufmann & } . E . Hazel (eds) Concepts a n d methods of biostratigraphy, pp. 3 - 22 . Dowden, Hutchinson & Ross, Stroudsburg, Pa. Hedburg, H.D. 1954. Procedure and terminology in strati­ graphic classification. 1 9th International Geological Con­ gress, Algiers, 1 952, Comptes Rendus No . 13, 205- 233. Holland, C . H . 1978 . Stratigraphical classification and all that. Lethaia 11, 85 -90. Holland, C.H. 1983 . Soviet and British stratigraphical classifi­ cations compared . Journal of the Geological Society 140, 845 - 847. Holland, C . H . 1986 . Does the golden spike still glitter? Journal of the Geological Society 143, 3-21 . Holland, C . H . , Audley-Charles, M . D . , Bassett, M . G . , Cowie, }.W., Curry, D . , Fitch, F.}., Hancock, } . M . , House, M . R . , Ingham, } . K . , Kent, P.E., Morton, N . , Ramsbottom, W.H.C., Rawson, P.F., Smith, D.B., Stubblefield, C.}., Torrens, H . s . , Wallace, P. & Woodland, A.W. 1978 . A guide to stratigraphical procedure. Geological Society of London

Special Report 11. Koren, T.N. 1984. Graptolite zones and standard stratigraphic scale of Silurian. 27th International Geological Congress Proceedings (Stratigraphy) 1, 47-76.

5 . 7 Zone Fossils M . G . BASSETT

of such taxa are then used for the name of the biozone itself; e . g . the Monograptus ludensis Biozone in the Silurian Period (based on a single index graptolite), the Geminospora lemurata-Cymbo­ sporites magnificus Biozone in the Devonian Period (based on a combination of spore taxa), and the Quenstedtoceras lamberti Biozone in the Jurassic Period (based on an ammonite species) . In general, the finer the taxonomic precision of the zonal index, the finer will be the degree of stratigraphic resol­ ution in correlation, so that, for example, a biozone identified on the basis of a species will normally give a greater degree of accuracy than one based on genera or higher taxonomic groups . Since different organisms evolve a t different rates and are subject to different environmental con­ straints, their potential as biozonal indicators will also differ considerably . Ideally, for use in accurate and refined biostratigraphy, zone fossils should have a number of well defined characters : (1) a short vertical range resulting from rapid evolution; (2) a wide horizontal distribution, preferably intercon­ tinental; (3) independence of facies control, as, for

The practical application o f biostratigraphy (Section 5 . 6) in correlating rock units carries with it the implication that the fossils used in any particular exercise have a time significance . In reality, the local time ranges of all fossils are likely to vary from section to section across the extent of their geo­ graphical distribution because of different evo­ lutionary and ecological factors that controlled origins, rates and extent of distribution, and extinc­ tions (Fig. 1 ) . Thus the ranges of fossils across a given area may well be diachronous in detail, but nevertheless, by careful collecting from accurately logged sections, it is possible to plot out the limits of successive faunas and/or floras that are represen­ tative of successive intervals of time . Biostrati­ graphic units built up in this way remain the primary tools for dating and correlating Phanerozoic sedimentary rocks throughout the world . The fundamental unit is the biozone, which is defined solely on the basis of its fossil content, without regard to either thickness or lithology. Fossils that characterize a particular biozone are termed zone fossils, or index fossils, and the names A

B

C

D

I

E

I

F

I

G

I

H

A

B

C

D

F

E

I

G

I

H

SYNCHRONOUS TIME PLANE

SYNCHRONOUS TIME PLANE

dispersal

I

I

Evolutionary origin

SYNCHRONOUS TIME PLANE

Left, Hypothetical vertical ranges of a fossil species through eight measured stratigraphical sections A - H . Right, Geographical distribution of the same species illustrating some of the factors responsible for its stratigraphical expression. (After Taylor 1987.) Fig. 1

466

467

5 . 7 Zone Fossils

�

INTERVAL BIOZONES

ASSEMBLAGE BIOZONES

Local range biozone

Assemblage biozone C Assemblage biozone B

Assemblage biozone A

� �

� --r+-

•

Contiguous assemblage biozones Consecutive range biozone (type l )

I

Consecutive range biozone (type 2)

_

l

-

-

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= i �I I � !] :

Ac=, biowne

example, in wind-borne spores and in free-swim­ ming as opposed to benthic organisms; (4) distinc­ tive morphological characteristics to ensure accurate identification; and (5) a high preservation potential, as in animals with hard shells or skeletons . It is rare for all these conditions to be met fully, but good examples of fossil groups that satisfy most criteria are the graptolites, ammonites, conodonts, planktic foraminifera, and spores. Fig. 2 illustrates some of the various categories of biozones that can be constructed using different data sets of vertical ranges of fossils (see, for example, Holland et al. 1978; North American Com­ mission on Stratigraphic Nomenclature 1 983; Taylor 1987) . In the local range biozone the total known range of the zone fossil defines the limit of the unit. The co-occurrence of overlapping taxa is used to de­ fine concurrent range biozones, in contrast to the con­ secutive range biozone where one (or more) of the zone fossils ranges through an interval unaccompanied by taxa that overlap with it at other levels . An acme biozone relies for definition on the recognition of a maximum occurrence of a fossil that might other­ wise range both higher and lower in the succession . In assemblage biozones the recognition of different taxa with varying vertical ranges forms the basis for definition, and in such cases the name of the biozone itself is generally based on one of the more common

.L _ _

-n T1jT I- }

ABUNDANCE BIOZONE

Fig. 2 Categories of biozones . (After Taylor 1987. )

I

-IL-'-,--}

Assemblage biozone Z Barren interval Assemblage biozone Y

: - Barren interval

:

Assemblage biozone X Barren intervi'l

Non-contiguous assemblage biozones

members . It is clear that a zone fossil is not neces­ sarily confined to the particular biozone that bears its name (Fig . 2) . The time-intervals represented by biozones, and thus their degree of accuracy in biostratigraphy, vary considerably throughout the geological column . Among the optimum levels of refinement currently available in Palaeozoic rocks are some graptolite biozones, which may give a resolution of correlation within one million years or less, whilst in the Mesozoic the time-span of some ammonite biozones and subzones may be as short as 200 000 250 000 years .

References Holland, C . H . , Audley-Charles, M . D . , Bassett, M . C . , Cowie, J.W., Curry, D . , Fitch, F.J., Hancock, J . M . , House, M . R . , Ingham,J . K . , Kent, P . E . , Morton, N . , Ramsbottom, W . H . C . , Rawson, P . F . , Smith, D . B . , Stubblefield, c.J., Torrens, H . s . , Wallace, P. & Woodland, A.W. 1978 . A guide to stratigraphical procedure . Geological Society of London Special Report 1 1 . North American Commission on Stratigraphic Nomenclature 1983 . North American Stratigraphic Code. Bulletin of the American Association of Petroleum Geologists 67, 841 - 875 . Taylor, M . E . 1987. Biostratigraphy and paleobiogeography. In: Boardman, R.S., Cheetham, A . H . & Rowell, A.J. (eds) Fossil invertebrates pp . 52 -66. Blackwell Scientific Publi­ cations, Oxford .

5 . 8 International Commission on Stratigraphy M . G . BASSETT

The International Commission on Stratigraphy (ICS) is the largest scientific body within the International Union of Geological Sciences (lUGS) . It is also the only organization concerned with the co-ordination of stratigraphy on a global scale . One of its major statutory objectives (Cowie et al . 1986) is the es­ tablishment of a standard, globally applicable strati­ graphic scale, which it seeks to achieve through the co-ordinated contributions of a network of Sub­ commissions, Working Groups, and Committees. It also organizes a number of conferences each year, and the results of these conferences are usually published. The precise definition of stratigraphic boundaries and their accurate correlation is a pre­ requisite of this work, particularly between divi­ sions of System, Series, and Stage rank, as a means of constructing an internationally agreed frame­ work within which geological events can be plotted both laterally and successively through time . In Phanerozoic rocks, fossils provide the chief means of correlating the sub-divisions of geological time and the boundaries between them . In practice, chronostratigraphic boundaries are defined at a unique point in a rock sequence at a specific locality, thus representing a unique instant in time and a standard against which other se­ quences can be correlated; this unequivocal method of definition is often called 'golden spike' strati­ graphy (see Holland 1986; Section 5 . 6) . Such a unique point defined within a rock section is now referred to as a Global Boundary Stratotype Section and Point (GSSP; Cowie et al. 1986), providing an immutable time signal within a globally standard stratigraphic scale, and the only place at that level in the scale where by definition time and rock co­ incide (Sections 5 . 6, 5 . 10 . 1 ) . The first inter-System boundary to b e defined and agreed internationally in this way was between the Silurian and Devonian systems (Martinsson 1977); in this case, and after considerable discussion of possible levels and appropriate sections through­ out the world by an international Working Group of the ICS, a point was selected in a succession at Klonk in Czechoslovakia which coincides with the first appearance in that section of the graptolite

Monograptus uniformis, taken to mark the base of the uniformis Biozone (Section 5 . 10.4) ; the strict defi­ nition of the GSSP is at a specific point within the rock sequence to mark the fixed point in time, and the base of the uniformis Biozone is not the defined level but is the datum used to correlate that point elsewhere . Similar subsequent decisions have been made for the Ordovician- Silurian (Section 5 . 1 0 . 3) and Pliocene - Pleistocene boundaries and for boundaries between Stage divisions within the Silurian and Devonian (Bassett 1985); fossils in­ volved so far as a main basis for correlation include graptolites, conodonts, and ostracodes . Within the ICS there are Subcommissions o f inter­ national experts that monitor the latest specialized disciplines within each geological System, Working Groups to consider the formal definition of remain­ ing inter-System boundaries, and Committees that carry out a variety of other standard-making strati­ graphical work. This complex working organization has evolved in the long history of the ICS since its origins in 1878 (Martinsson & Bassett 1980; Cowie et al. 1986, p. 4) . Most International Geologi­ cal Congresses have had commissions and com­ mittees, with various names and with various durations, that have been concerned with inter­ national co-operation in stratigraphy, stratigraphic classification, and stratigraphic terminology. At the 11th Congress, Stockholm, 1910, a Commission on a Lexicon of Stratigraphy was created . This Com­ mission functioned modestly through many sub­ sequent Congresses. At the 19th Congress, Algiers, 1952, however, its name was changed to Com­ mission on Stratigraphy and it was reorganized to include two Subcommissions: a Subcommission on the Lexicon of Stratigraphy and a Subcommission on Stratigraphic Nomenclature . Since that time the Commission on Stratigraphy has functioned con­ tinuously and many new Subcommissions have been added . In May 1 965, the Commission applied formally for admission to the lUGS and was accepted as a commission of the lUGS . At that time the membership of the Commission was reduced dras­ tically from 150 - 200 members to consist only of its officers and the presidents of its Subcommissions .

468

5. 9 International Geological Correlation Programme In its overall objective to clarify and co-ordinate principles of stratigraphic procedure, and to pro­ duce a unified nomenclature for a standard strati­ graphic scale as a means of documenting global events unambiguously, the ICS also incorporates data from all other branches of stratigraphy, such as quantitative stratigraphy, magnetostratigraphy, chemostratigraphy, and geochronometry, to inte­ grate with the biostratigraphic methods empha­ sized here and together they form the embracing discipline of holostratigraphy.

469

References Bassett, M . G . 1985 . Towards a 'common language' in strati­ graphy. Episodes 8, 87-92. Cowie, J.W., Ziegler, W., Boucot, A.J., Bassett, M.G. & Remane, J. 1986 . Guidelines and statutes of the Inter­ national Commission on Stratigraphy (ICS) . Courier Forschungsinstitut Senckenberg 83, 1 - 14. Holland, C H . 1986 . Does the golden spike still glitter? Journal of the Geological Society 143, 3 - 21 . Martinsson, A. (ed . ) 1977. The Silurian - Devonian Boundary. International Union of Geological Sciences, Series A, No . 5. Martinsson, A . & Bassett, M.G. 1980 . International Com­ mission on Stratigraphy. Lethaia 13, 26.

5 . 9 International Geological Correlation Programme J . W . C OWIE

Introduction In its life of over 15 years this joint programme of the International Union of Geological Sciences (lUGS), an independent non-governmental scien­ tific body, and the United Nations Educational, Scientific and Cultural Organization (UNESCO) have sponsored a considerable body of geological research . This has been achieved in a number of ways (Skinner & Drake 1987) : 1 Through the creation of a professional advisory

secretariat with permanent headquarters in Paris and with, more recently, regional offices in various parts of the world to serve particularly remote (from Paris) and/or developing regions. 2 By means of grants to International Geological Correlation Programme (IGCP) projects whose scientific programmes and logistics have been re­ viewed and submitted through a Scientific Com­ mittee of volunteer, unpaid geologists from many parts of the world . (Finance comes to the IGCP from national government subscriptions on a codified basis . ) These project grants are relatively small but are valuable 'pump-primers' or 'seed-money' serving as a validating and commendatory mechan­ ism to attract other funds from national funding bodies, learned societies, geological surveys, commercial companies, and universities . 3 The individual IGCP projects are required, if they wish to continue to receive annual grants, to report

in good time each year to the IGCP Secretariat which briefs the Scientific Committee and the Board of IGCP for their respective annual meetings in February. At these meetings decisions are made regarding overall policy, guidance for projects (through their project leaders), and level of funding for the coming year. The IGCP arose from a conference in Czechoslo­ vakia in 1967 to meet the need for a more concerted international effort to solve some of the fundamen­ tal geological problems with which the lUGS is concerned . Through 1968 and 1969 the proposal moved forward . A final draft, completed in 1971, was adopted by the Council of the lUGS and the General Conference of UNESCO; this launched the IGCP as a co-operative venture, and its statutes were approved in 1972 . In May 1973 the IGCP Board held its first session at the UNESCO headquarters in Paris with Sir Kingsley Dunham (U .K.) as Chair­ man . W . B . Harland (U .K.) had acted as Secretary of the lUGS Co-ordinating Panel during the formative period and F . Ronner was appointed as Secretary of the 1973 Board .

Aims and scope The principal goal of the IGCP is to encourage international research on geological problems re­ lated to the identification and assessment of natural

470

5 Taxonomy, Phylogeny, and Biostratigraphy

resources and the improvement of man's environ­ ment. Continuing IGCP aims have been to stress the scientific achievements of the projects, improv­ ing man's environment, access to mineral resources, assistance in co-operation and communication be­ tween scientists from different regions, and the transfer of knowledge to developing countries . Assessments of the IGCP have been published by Reinemund & Watson (1983) and Skinner (1987) . The scientific scope of the IGCP has varied little since 1973; changes in emphasis have been subtle and have largely reflected changes in global geologi­ cal policy and aims, with a slight shift, perhaps, from more academic, basic science to more applied, man-orientated aspects . Pure palaeobiology has not really been a part of the IGCP, but stratigraphy (including biostratigraphy) has played a significant role . The following projects are worthy of note in this context: 1 Precambrian - Cambrian boundary (Project 29) . 2 Ecostratigraphy (Project 53) . 3 Biostratigraphic datum-planes of the Pacific Neo­ gene (Project 1 14) . 4 Upper Precambrian correlations (Project 1 18) . 5 West African biostratigraphy and its correlations

(Project 145) .

6

Phosphorites of the Proterozoic- Cambrian (Project

156) .

7 Early organic evolution and mineral and energy resources (Project 157) . 8 Stratigraphic methods as applied to the Proterozoic record (Project 179) . 9 Rare events in geology (Project 199) . 10 Global biological events in Earth history (Project

11 12

216) .

Floras of the Gondwanic continents (Project 237) . Stromatolites (Project 261 ) .

The range o f topics with a palaeobiological em­ phasis is illustrated by those listed 10- 12. New projects will probably be added by the IGCP, but there may be no new palaeobiological projects per se coming forward and this is a gap which palaeo­ biologists may wish to see filled - 12 out of 264 Projects in 15 years with only varying commitment may be considered too small a proportion of this international key programme .

Examples of palaeobiological projects Project 261 on Stromatolites was started in 1987 with a meeting in Cardiff, U.K. Its full title is The biostratigraphical and environmental significance of stroma to lites and other microbially derived

organosedimentary structures through space and time' . The aim is to understand microbial evolution and the factors affecting stromatolite morpho­ genesis, to establish their classification, biostrati­ graphic potential, and role in forming mineral and petroleum deposits . The approach is multi­ disciplinary . Project 237 on Floras of the Gondwanic continents was started in 1986 and held a key meeting in Silo Paulo, Brazil at the 7th Gondwana Symposium in July 1988 . The primary objective is to produce a general, up-to-date summary of the Upper Silurian to Lower Tertiary flora of the Gondwanic continents . An interesting aspect of IGCP work is the exploi­ tation of training opportunities in developing countries via international co-operation of experi­ enced scientists from many countries . In 1986 at the University of Silo Paulo a four-month training session was mounted in paleobotany and paleo­ phytogeography. Further courses in 1987 and 1988 also involved African participants . Project 216 on Global biological events in Earth history has, in its activities in 1986 and 1987, aroused very wide interest indeed and is probably the IGCP Project which holds the most interest for palaeobio­ logists in general. The project arose from a pro­ gramme of the International Palaeontological Association (IPA) and is concerned with world-wide, traceable, exceptional changes ('events') within the biosphere . It aims at a better understanding of the dependence and interdependence of processes and extraordinary events in the biosphere, geosphere, and atmosphere . Global bioevents fall into several categories of pattern: innovation-events (especially important in the Precambrian and Early Phanero­ zoic), radiation events, spreading events, and extinction events (which may not be extremely short-term but may occur stepwise) . Cyclic and acyclic processes are given special attention in their possible overlap . Probable causes are either cosmic (revolution of the Solar System within the Galaxy and impact of cosmic bodies; Section 2 . 1 2 . 2) or bio­ logical and abiotic (sea-level, oceanic physical and chemical composition, climate, oceanographic para­ meters; Section 2 . 12 . 1 ) . Some causes may be cata­ strophic but resulting from combination with unstable or perturbed conditions . In 1988 an inter­ national meeting of Project 216 entitled 'Abrupt changes in the global biota' was held in Boulder, U . S . A . Already the Project's 15 or so pages of biblio­ graphy indicate the opportune and seminal aspect of this successful palaeobiological IGCP activity.

5. 1 0 Global Boundary Stratotypes References Reinemund, J.A. & Watson, J.V. (eds) 1983 . Science resources and developing nations : a review and a look into the future, 1978-1982. Geological Correlation, Paris, Special Issue, 1 - 166.

471

Skinner, B.J. (ed . ) 1987. Scientific achievements, International Geological Correlation Programme IGCP. Geological Cor­ relation, Paris, Special Issue, 1 - 123. Skinner, B.J. & Drake, c . L . 1987. On the IGCP : an unacclaimed success story. Geotimes, November, 1 1 - 13.

5 . 10 Global Boundary Stratotypes

5 . 10 . 1 Overview J . W . C OWIE

The most basic property o f rocks which i s utilized in stratigraphy is lithology; lithostratigraphy is con­ cerned with the organization of rock strata into units based on their lithological character . Strati­ graphy is also concerned with the organization of strata into two other types of units, however: (1) biostratigraphy, based on fossil content; and (2) chronostratigraphy, based on age relations . The latter, because of the nature of time, is the most abstract . Chronostratigraphic major boundaries have in recent decades been studied mainly by international working groups and projects (Lafitte et al. 1972; Harland 1973; Hedberg 1976; Bassett 1985) . The different properties of rocks give rise to other branches of stratigraphy such as magneto­ stratigraphy, chemostratigraphy, stable isotope chemostratigraphy, and seismostratigraphy . This splitting of the subject into branches can lead to considerable complexity because the changes in a rock stratal succession based on one property may not coincide with those for another; different sets and types of units may be needed to assemble a unified time-scale . The newer term holostratigraphy covers the study of all aspects together and the general unity of strati graphic studies should not be overlooked. There is no consensus view of the principles and practice of stratigraphy . The position outlined here is that currently adopted by the International Com­ mission on Stratigraphy of the International Union of Geological Sciences, which, in the true spirit of

science, will probably evolve or change radically in the next few decades. The most reliable systems of stratigraphy deal with global processes which are universal, unidirectional in the sense of irreversible (time sequences can only be read one way) and non­ recurrent, and non-repeatable . Included here, most significantly, is the evidence from biological evo­ lution (sequential) and nuclear decay (metric) . Bio­ logical evolution interacts through geological time with other factors, but is the main indicator of the direction of the arrow of time, of prime polarity . The evidence available so far shows that it cannot be stopped and reset . Nuclear decay also has po­ larity, but, unlike biological evolution, it can be stopped and reset; additionally, it has the great virtue of numeracy . Geochronometry has particular attraction for geoscientists working in unfos­ siliferous or sparsely fossiliferous rocks, but bio­ stratigraphy gives the most useful and, at the present stage of research, generally the most accurate framework. Those who work mainly with the earlier part of the Proterozoic Eon rocks and the Archaean Eon rocks find little help from the stratigraphic methods frequently used in the Phanerozoic Eon - in par­ ticular with respect to palaeobiology and bio­ stratigraphy . In attempting to establish a global Precambrian chronostratigraphy current ideas favour a chronometric subdivision based upon intervals of 'geological convenience' . Such a chrono­ metric approach does not rule out the possibility of separate thematic time-scales - biostratigraphic, magnetostratigraphic, chemostratigraphic. This applies especially to the later part of the Proterozoic where palaeobiological evidence is available . The Archaean- Proterozoic Boundary is placed at 2500

472

5 Taxonomy, Phylogeny, and Biostratigraphy

Ma . A tripartite subdivision of the Proterozoic in eras with boundaries at 1 600 Ma and 900 Ma is widely recommended . Today, stratigraphy i s a subject in a dynamic phase of development, with diverse emphases on aspects like unique or recurrent cyclic events (event stratigraphy), such as ash falls, eustatic changes, glacial deposits, appearance or disappearance of a particular biota, and evidence of impacts of extra­ terrestrial bodies . If these events can be shown to have global and isochronous effects, so that they are not merely parochial and diachronous masquerades, then they can be uniquely valuable in elucidating Earth history . Cyclicity is still being sought in the modem search for the 'pulse of the Earth' . Adjec­ tives attached to stratigraphy proliferate, indicating renewed interest and involvement with strati­ graphy as the keystone of the geological sciences - ecostratigraphy, seismic stratigraphy, chemo­ stratigraphy, event stratigraphy, biostratigraphy, magnetostratigraphy, sequence stratigraphy, and others (Berry 1984) . International stratigraphy is much concerned with efforts to correlate standard global Series, Stages, and Systems, and a major part of this work has been to define boundaries between them (Fig . 1 ) . Accurate communication without definition is impossible . A Boundary Definition utilizing a unique point in a rock sequence represents (if correctly selected), as nothing else in geology can, a unique instant of time; it defines unequivocally a standard against which other sequences can be correlated by the analysis of all available data . Biological! palaeontological species are subjective and the full range is unknown - because of incomplete research, or incompleteness of the geological record . This shortcoming can be overcome by using several independent groups of fossils to correlate faunal! floral assemblages (Glaessner 1 984) . It is salutary to recall that matters of positive science, which concern 'nature', require discovery, and apply some test of truth, should be distinguished from matters of normative science, which are regulated by man as part of his method of understanding nature and which apply tests of correctness and utility . The global stratigraphic scale (chronostratigraphy) is a norm which can be legitimately established by inter­ national agreement through an agreed voting pro­ cedure . It can be argued that choices in international stratigraphy should violate historical priority as little as possible, but this consideration can often be overridden by the higher priority of going for the best and making progress . Confusing historical

Fig. 1

The cover of a publication produced by the Subcommission on Cretaceous Stratigraphy.

precedents may need to be set aside by an authori­ tative international decision (which is very likely to violate some established usage) . Historical geology depends on positional relation­ ships of rock and mineral bodies and identification of the Earth's evolutionary trends . The importance of the boundary stratotype lies in its role as a future anchor to which all subsequent correlations can be tied, even if new palaeobiological or physical methods become available, because it is the only place where we actually know (by definition) that time and rock coincide within our classification . A Boundary Stratotype Point defines, without doubt, an instant of geological time . A horizon will, at the Global Stratotype Section and Point (GSSP) locality, contain the Point, but the horizon may, traced laterally, be diachronous (cutting across time­ planes) and may drift away from the instant of time defined by the point. The GSSP is the standard and is unique . The correctly selected GSSP gives an actual point in rock and is therefore not an abstract concept - all other methods can prove to be dia­ chronic . It will be expected to remain fixed in spite of discoveries stratigraphically above and/or below . The main criterion is that any horizon and point selected must be capable of being correlated over

5. 1 0 Global Boundary Stratotypes wide areas by any or all available methods . In a world which is not ideal, it is most unlikely that all selected stratotype points can meet all the ideal requirements; stratigraphy must therefore be a practical subject which responds to the needs of working geologists (Holland 1986) . GSSPs allow maximum flexibility with the use of multiple hypotheses to give minimum ambiguity and the greatest likelihood of stability. It is necessary to emphasize that each GSSP is the designated type of a stratigraphic boundary identified in published form and marked in the section as a specific point, constituting the standard for the definition and recognition of the stratigraphic boundary between two named global standard chronostratigraphic units . The type locality of a GSSP is the specific geographical locality in which the stratotype is situ­ ated.

Aspects to consider in the selection of

a

GSSP

Of great importance is the relationship of a strato­ type section and point sequence to globally sig­ nificant marker horizons in the immediate and accessible region, e . g . faunal or floral zone assem­ blages stratigraphically above or below the strato­ type point, climatic markers such as tillites, and other factors assisting long-range (preferably glo­ bal) correlation. Correlation must precede, accom­ pany, and follow definition of a boundary . The choice of an appropriate boundary level for the point is only possible where a marker horizon has proved to be isochronous within the limits of pre­ cision attainable by stratigraphic methods . Auxi­ liary marker horizons as close as possible to the boundary level will give good approximate strati­ graphic positioning where and when the primary marker is missing. Other aspects to be considered include : 1 Continuity o f sedimentation through the bound­ ary interval - preferably a marine succession with­ out major facies change . A continuous monofacial succession (or one with only rapidly alternating and repeating facies changes) will reduce possible errors resulting from stratigraphic gaps . It will also limit the occurrence of facies fossils and appearances and disappearances associated with environmental change rather than biological evolution of lineages . 2 Completeness o f exposure : not in an isolated position but with a succession which can be followed easily - above and below the GSSP, and preferably laterally as well . 3 Adequate thickness of sediments .

473

4 Abundance and diversity of well preserved fossils : appearances and disappearances of single fossil species may be diachronous and therefore a bad guide for the location of a GSSP . Multispecies fossil zones (e . g . faunal assemblages) may be preferable . Taxa which are palaeoecologically tied to facies should be excluded from consideration (although all fossils are to some extent facies fossils) . In order to minimize possible effects of environ­ mental controls on different fossil groups, recog­ nition of the boundary level should preferably be based on all available faunal and floral data . The selection of appropriate fossils will vary greatly in different parts of the geological column. Ideally, selection of a point within an evolutionary lineage is desirable but recognition of such lineages can be subjective and not necessarily more accurate than the recognition of a particular assemblage zone . Such decisions must be left to the experts in each case . Autochronology, i . e . a single species taken out of a phylogenetic lineage (with its predecessor and successor known in detail) as the biological way of approaching a boundary free of ecological, facial, or sedimentary disturbing effect, may be a powerful tool when available . 5 Favourable facies for the development of wide­ spread, reliable, and time-significant correlation horizons : this requires that the GSSP should not be in or close to conglomerates, breccias, olistostromes, turbidites, or remanie deposits . This should, as far as possible, eliminate variation of chronostrati­ graphic or chronometric age within the stratotype section near the stratotype point. Even if, for example, fossils in derived blocks and surrounding matrix appear to be of the same species and age, the danger exists that new techniques or new finds (palaeobiological or physical, such as magneto­ stratigraphy) might discriminate between the blocks and matrix, introducing an unacceptable imprecision. 6 Freedom from structural complication, metamor­ phism, or other alteration: currently the question of exotic accreted terrains is pressing, but the problem of the relationship between present and past pos­ ition may not adversely affect global stratigraphy . 7 Freedom from unconformities : an obvious bound­ ary should be suspect . Either it is too obvious because there is a marked change in lithology or because there is a marked change in fauna or flora . In either instance the change may imply a time­ break, and consequently an unsuitable horizon at which to fix any time definition; no disconformities, unconformities, cryptic paraconformities, or time-

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5 Taxonomy, Phylogeny, and Biostratigraphy

breaks in sedimentation any longer than a brief diastem can be tolerated close to a GSSP . 8 Amenability to magnetostratigraphy and geo­ chronometry: these factors are probably the most important for future work and some would argue that no GSSP should be accepted without one or both .

Boundary stratotype procedure

2

Correlation on a global scale . Completeness of exposure . 4 Adequate thickness of sediments . 5 Abundance and diversity of well preserved fossils . 6 Favourable facies for widespread correlation. 7 Freedom from structural complication and meta­ morphism. 8 Amenability to magnetostratigraphy and geo­ chronometry . 3

One of the main aims of the Boundary stratotype procedure is to attain a common language of strati­

Accessibility and conservation. These two topics are

graphy that will serve geologists world-wide and avoid petty argument and unproductive contro­ versy . Development of a standard global strati­ graphic scale which is stable for a considerable period of time is the objective . Testing can then proceed . If new developments demand revision, this can be considered in exceptional circumstances such as: (1) permanent destruction or inaccessibility of an established stratotype; or (2) violation of ac­ cepted stratigraphic principles . In the overwhelming majority of cases in the Phanerozoic Eon, correlation must precede the definition of a boundary . Unless preliminary choices are made, however, progress may be slow as the process of testing a candidate or the competition between candidates may be the stimulus required for improvement of needed correlation techniques and of the correlation itself. Correlation must pre­ cede the selection of boundary stratotype candidates to a considerable extent, but in practice the proce­ dure may be complex . The finding of the best strati­ graphic level and best geographical site may have to proceed in tandem for a time . Correlation to a satisfactory degree is necessary but improvements in correlation should continue after a boundary stratotype has been selected. In the Phanerozoic Eon, where the prime polarity factor is biological evolution, boundaries will normally be guided in their definition by chronostratigraphy (led by bio­ stratigraphy), but in the Proterozoic and Archean Eons guidance will be chronometric at the present stage of research . Chronostratigraphy can be ex­ pected to be used increasingly for boundaries late within the Precambrian successions . It would be unwise (or impossible) to specify which criteria are essential and which are desirable up and down the geological time-scale, because of the multiplicity of criteria involved, and the vari­ ation in circumstances . Only a brief preliminary checklist can be suggested : 1 Explicit motivation for the preference .

contrasting but complementary factors . Recent ex­ perience has shown that if access to an important outcrop is too easy and unrestricted then excessive collecting (even vandalism and plunder) may de­ stroy the outcrop . Conservation and some restriction is therefore necessary in developed regions . Conser­ vation in more remote regions may be easier but this depends on regional geological activity by outsiders . A problem for access/conservation may be weathering, e . g . heavy rainfall can form rapid mud flows from a marly sequence, frost can form screes which soon cover an outcrop, and outcrops on sea coasts may be particularly subject to rapid erosion . There must be no insuperable physical and/or political obstacles to access by geologists of any nation, and access should preferably be afforded without great expense and ideally without much bureaucracy . At the International Geological Con­ gress in Moscow (1984) it was agreed that a reason­ able amount of collecting must be possible at a stratotype section . Although it is difficult for any group of geologists to commit any nation or organ­ ization to guarantee access and conservation for the indefinite future, total accessibility must assume considerable importance . If a GSSP were found to be inaccessible in the future, this would be a very powerful argument for a reassessment of the geo­ graphical location . There is a metamorphosis once a GSSP has been ratified by the International Union of Geological Sciences: 1 Beforehand, all methods of correlation are enlisted to define a globally valid GSSP and to distinguish between what belongs to System X and what be­ longs to System Y. 2 After the decision the GSSP can be used to indi­ cate without ambiguity what constitutes earliest System X and latest System Y. Correlation has in any case to precede the definition of a GSSP . Pos­ sibilities of correlation should be tested simul-

5. 1 0 Global Boundary Stratotypes taneously, of course, at different levels close to the boundary . There is no conflict between the global boundary stratotype concept and globaC isochronous, event stratigraphy . The combination of global environ­ mental change and major biotic changes (which may be caused by biological evolution) brings together lithostratigraphy and biostratigraphy to provide event stratigraphy . Stratotypes bring stab­ ility by an agreed point in rock representing a unique instant of time . The ultimate reference is to rock and not to abstractions . In this work during the past decade or two, much inspiration and guidance has been derived by the international geological community from the brilliantly-expressed published results of the Silurian - Devonian Boundary Committee which have the great virtue of being based on practical experience in actually defining a GSSP (McLaren 1977; see also Section 5 . 10 .4) .

References Bassett, M . G . 1985 . Towards a 'common language' in strati­ graphy. Episodes 8, 87-92. Berry, W.B.N. 1984. The Cretaceous-Tertiary boundary the ideal geologic time scale boundary? Newsletter on Stratigraphy 13, 143 - 155. Glaessner, M.F. 1984. The dawn of animal life. Cambridge University Press, Cambridge . Harland, W.B. 1973 . Stratigraphic classification, terminology and ut;age . Essay review. Geological Magazine 110, 567574. Hedberg, H.D. (ed . ) 1976. International stratigraphic guide. Wiley Interscience, New York. Holland, C.H. 1986 . Does the golden spike still glitter? JournaL of the GeoLogical Society 143, 3 -21 . Lafitte, R . , Harland, W . B . , Erben, H.K., Blow, W.H., Haas, W., Hughes, N . F . , Ramsbottom, W . H . C . , Rat, P., Tintaut, H. & Ziegler, W. 1972 . Some international agreement on essentials of stratigraphy. Geological Magazine 109, 1 - 15 . McLaren, D.J. 1977. The Silurian -Devonian Boundary Committee . A final report, pp. 1 - 34. In: A. Martinsson (ed . ) The Silurian - Devonian Boundary. International Union of Geological Sciences, Series A, No . 5. E . Schweizerbart'sche Verlagsbuchhandlung, Stuttgart.

475

5 . 10 . 2 Precambrian - Cambrian J . W . COWIE

Historical background The base of the Cambrian System, which is perhaps better termed the 'Precambrian - Cambrian Bound­ ary' to emphasize the role of Precambrian studies as well as Cambrian research, is proving a difficult major geological horizon for which to establish a global standard . Interest was somewhat muted in the nineteenth century when so many enthralling problems concerning the younger parts of the geo­ logical column engaged attention . The relatively abrupt appearance of skeletalized fossils near the base of the Cambrian system is perhaps the greatest palaeobiological enigma, and this did not escape the attention of early geologists . It was not until the twentieth century, however, that much progress was made, as a consequence of the acceleration in exploration of the Earth's surface and the examin­ ation of sedimentary successions spanning the Precambrian - Cambrian transition (equivalent in age for most geologists to the Proterozoic Eon ­ Phanerozoic Eon transition) . In 1835 A. Sedgwick named the 'Cambrian Series' but his Lower Cambrian succession was largely without a fossil basis and would now be considered to include some Precambrian rocks as well. From the time of Cuvier in the eighteen-thirties it was assumed that natural breaks divided rocks in a world-wide pattern and that the 'Cambrian' rested un conformably on 'Archaean and Precambrian basement series' . Thus the base of the Cambrian was stratigraphically coincident with the uncon­ formity first seen below the 'Cambrian' trans­ gression . Vestiges of these ideas still persist and may yet be rejuvenated in event stratigraphy . Even as late as the nineteen-forties it was a tradition to regard, in the absence of other evidence, rocks without fossils at this level as Cambrian in age . Three decades ago workers equated the first horizon with trilobites ('Olenellus Zone') with the base of the Cambrian . The Archaean and Proterozoic Eons were grouped into rock units limited by unconform­ ities that were thought to have a world-wide validity and occurrence . In recent decades, more and more successions have been described with apparently continuous sequences ranging from fossiliferous Cambrian rocks down into unfossiliferous strata of

476

5 Taxonomy, Phylogeny, and Biostratigraphy

a lithological facies which could be expected to yield fossils but do not. A 'Symposium on the Cambrian System and its Base' at the 1956 Inter­ national Geological Congress in Mexico was fol­ lowed by a conference in Paris on the Precambrian ­ Cambrian Boundary in 1957. Further discussion took place in Copenhagen at the International Geo­ logical Congress in 1960 . Research by Soviet geo­ logists published in the nineteen-sixties was responsible largely for the establishment in 1972 (through stimulus from V.V. Menner, W . B . Harland, M . F . Glaessner, c.J. Stubblefield, and J . W . Cowie) of the Working Group on the Precambrian ­ Cambrian Boundary by the lUGS' s International Commission on Stratigraphy (ICS) (Section 5 . 8 ) .

Precambrian - Cambrian Boundary Working Group At the first meeting in Yakutia, eastern Siberia, U . s . s . R . , it was agreed that the Working Group should seek international agreement on the defi­ nition of the Precambrian - Cambrian Boundary in litho-, bio-, and chronostratigraphic terms based on a point in a standard rock sequence (Global Strato­ type Section and Point - GSSP; Section 5 . 10 . 1) coupled with elucidation of the significant palaeo­ biological transitions occurring at, or about, this stage in the Earth's history. Selection of the GSSP would be based on biostratigraphy but all possible methods of correlation should be enlisted (Cowie 1985) . Up to 100 members from 20 countries have been involved in the Working Group, all recruited as individuals with relevant expertise, and at present there are 24 Voting Members . All serve as individual scientists and not as delegates of any nation or institution. From 1974 to 1988 the Working Group also functioned as IGCP Project 29: 'Precambrian ­ Cambrian Boundary' . From 1972 to 1987, a series of meetings was or­ ganized to examine and discuss Precambrian ­ Cambrian Boundary sections . Plenary sessions and workshops were held in Montreal, Canada (1972), Paris, France (1974), Moscow, U . s . S .R. (1975), Leningrad, U . S . S . R . (1976), Sydney, Australia (1976), Beijing, China (1978), Paris, France (1980), Golden, Colorado, U . S .A . (1981), Kunming, China (1982), Bristol, U . K . (1983), Moscow, U . S . s .R. (1984), Uppsala, Sweden (1986), St. John's Newfoundland Canada (1987), and south China (1987) . Field meetings were also held, involving both examination of sections and discussions leading to

subsequent research with local geologists . The fol­ lowing areas were visited : east Siberia, U . S . S .R. (1973 and 1981), Normandy and Brittany, France (1974), Ural Mts . , U . S . S .R. (1975), Georgia, U . S . S . R. (1975), Anti Atlas Mountains of Morocco (1975 and 1976), Flinders Ranges in South Australia (1976), Iberian Peninsula of Spain and Portugal (1976), central and south China (1978 and 1982), eastern Newfoundland, Canada (1979), Mackenzie Moun­ tains, Canada (1979), Nevada - California, U . S . A . (1981), Wales and England (1983), south Sweden (1986), Newfoundland (1987), and south China (1987) (Fig. 1 ) . The Precambrian- Cambrian transition i s not sig­ nalled only by the skeletalization of fossil hard parts but is part of a major physical-chemical-biological change over (possibly an 'explosion') shown also by the following (and other) changes and signals : 1 Decrease i n dolomite accumulation. 2 Sharp drop in stromatolite formation and change of morphology. 3 First widespread appearance of red biogenic lime­ stones. 4 Global accumulation of large phosphorite de­ posits (especially in the U . S . S .R., People's Republic of Mongolia, and China, but also elsewhere) . 5 Considerable changes in the morphology and bio­ logical 'programming' of trace fossils. At the 1983 Bristol meeting, candidates for the Global Stratotype Section and Point were discussed in some detail, and three were selected for further consideration: Ulakhan-Sulugur on the Aldan River in east Siberia, U . S . S . R . ; on the Burin Peninsula, of eastern Newfoundland, Canada; and at Meishucun in Yunnan Province, southern China. At that time it was decided that the boundary stratotype should be placed as close as practicable to the lowest known appearance of diverse shelly fossils with a good potential for correlation (Luo Huilin et al. 1984; Rozanov 1984; Narbonne 1987) . These three candidates remain as prime choices in 1989 but new areas may well present important stratotype candidates in the future . They include the Olenek uplift region of northern Siberia (near the Anabar massif) and the Elburz mountains of Iran; the latter, in particular, has rich fossiliferous strata near the putative boundary and the former has great potential for correlation globally. In 1987 a new GSSP candidate was presented by the Canadian and u . s . members of the Working Group at a slightly different level to the former Newfoundland candidate and guided by trace fos­ sils as well as body fossils . It was claimed thal

5. 1 0 Global Boundary Stratotypes

477

Sta b l e Preca m b ri a n s h i e l d s

Current geography o f some important Precambrian - Cambrian boundary sections (circled) and Precambrian cratons (stippled) . 1, North Wales, Shropshire and Nuneaton, England . 2, Bornholm and southern Sweden. 3, Northern Poland . 4, Troms, Norway, and Finnmark. 5, Onega Peninsula. 6, Sukharika river, Igarka region. 7 - ID, Anabar region: 7, Eriechka river; 8, Kotui river; 9, Fomitch and Rassokha rivers; 10, Kotuikan river. 11, Olenek uplift. 12, Chekurovka, lower reaches of Lena river. 13, middle reaches of Lena river. 14, Aldan river. 15, Kuznetask Alatau and northeastern Sayan . 16, Karatau, southern Kazakhstan. 17, Salt Range and Hazara district, Pakistan. 18, Mussoorie, Lesser Himalaya of India. 19, Meishucun, near Kunming, eastern Yunnan. 20, Maidiping, near Emei, southwestern Sichuan . 21, Northwestern Guizhou . 22, Southwestern Shaanxi. 23, Eastern Yangtze gorges, western Hubei. 24, Western Xinjiang. 25, Salanygol, Mongolian People's Republic. 26, Ediacara, Flinders Range, South Australia. 27, Mount Lofty and Yorke Peninsula, South Australia. 28, Amadeus and Georgina Basins, Northern Territory. 29, Nama Group, Namibia. 30, Anti Atlas and High Atlas, Morocco . 31, Sierra Morena and Montes de Toledo, Spain. 32, Cantabria and Asturia, northern Spain. 33, Montagne Noire, Herault, France . 34, Brioverian of Normandy and Brittany, France . 35 . Fortune Bay, Burin, Bonavista, and Avalon Peninsulas, southeastern Newfoundland . 36. St John, New Brunswick. 37, Nahant and North Attleborough, Massachusetts. 38, Carborca, Sonora, Mexico. 39, Mount Dunfee, Nevada and White Inyo Mountains, eastern California. 40, Mackenzie, Selwyn, and Wernecke Mountains of Yukon and Northwest Territories, northwestern Canada. 41, Corumba Group, State of Matto Grosso, Brazil. 42, Elburz Mountains, northern Iran . Localities 5 - 1 6 are in the U . 5 .5.R. and 19-24 are in the People's Republic of China . (After Brasier in Cowie & Brasier 1989. ) Fig. l

although the Precambrian - Cambrian boundary marks a fundamental change in Earth history with the first development of abundant skeletal and bio­ turbating organisms, and there is general agreement with the principle of placing the boundary ' . . . as close as practical to the first appearance of abundant shelly fossils . . . ' , marked provincialism of the earliest skeletal fossils and their virtual restriction to carbonate facies have hampered global correlation in the boundary interval . Trace fossils are especially common in siliciclastic facies, in which shelly fossils typically are rare and poorly preserved. Correlation in siliciclastic facies is critical, as these deposits comprise nearly 70% of exposed rocks in the bound-

ary interval . Crimes (in Cowie & Brasier 1989) has outlined three globally-correlatable trace fossil zones that occur below the lowest trilobites .

Future research It is clear that much research remains to be done on the palaeobiology of the Precambrian- Cambrian (Proterozoic- Phanerozoic) transition. Future work should include : 1 Integration of a global table of correlation by further documentation of stratotype sections using all available techniques . 2 Calibration of trace fossil data with the earliest

5 Taxonomy, Phylogeny, and Biostratigraphy

478

skeletalized body fossils, particularly in Asia, with revision and updating of range charts . These tables also should incorporate First Appearance Datum (FAD) and Last Occurrence Datum (LOD) of the main skeletal fossils, ichnofossils, and acritarchs, and evidence from sea-level curves, geochemistry (including stable isotopes), and magnetostrati­ graphy . 3 While not departing greatly from previous criteria regarding the stratigraphic level chosen for the Global Stratotype Section and Point, it seems agreed: (i) the level should be traceable into carbonate plat­ form successions in Asia through the early skeletal fossil sequence and/or by chemostratigraphy, magnetostratigraphy, or sequence - event strati­ graphy; (ii) the level should also be traceable into clastic platform successions linking with the trace fossil sequence and/or chemostratigraphy, mag­ netostratigraphy, or sequence - event stratigraphy; and (iii) tracing of the level into deeper sedimentary basins could be achieved through chemostrati­ graphy, magnetostratigraphy, and sequence - event stratigraphy .

References Cowie, J.W. 1985 . Continuing work on the Precambrian­ Cambrian Boundary. Episodes 8, 93-97. Cowie, J.W. & Brasier, M.D. (eds) 1989 . The Precambrian ­ Cambrian Boundary. Oxford University Press, Oxford . Luo Huilin, Jiang Zhiwen, Wu Xiche, Song Xueliang & Ouyang Un 1984. Sinian - Cambrian Boundary strata section at Meishucun, Jinning, Yunnan, China . People's Publishing House, Yunnan . Narbonne, G . M . 1987. Trace fossils, small shelly fossils and the Precambrian - Cambrian Boundary . Episodes 10, 339 340 . Rozanov, A. Yu 1984. The Precambrian - Cambrian Boundary in Siberia. Episodes 7, 20-24.

established a stratigraphy both in southern Scot­ land and in Wales, primarily by employing grapto­ lites to develop biostratigraphic subdivision and correlation (Fig . 1 ) . I t was soon recognized that both upper and lower boundaries of the system were marked by wide­ spread breaks in sedimentation. The global re­ gression during the Late Ordovician is now thought to be related to a glaciation in the Southern Hemi­ sphere; evidence was first documented in Northern Africa, but periglacial deposits have since been found in South Africa, South America, Spain, and possibly northwest France (Rong in Bruton 1984) . Brenchley and Newall (in Bruton 1984) es­ timated that the glaciation extended northwards to 400S, with a high sea-level stand during the Rawtheyan Stage, global regression in the Early Hirnantian Stage (Paraorthograptus pacificus/ Climacograptus? extraordinarius Zone), then dramatic eustatic rise during the Glyptograptus persculptus Zone . Evidence for such eustatic change is seen in many areas, where late Ordovician regressive sequences are commonly followed by a hiatus equivalent to the C? extraordinarius Zone or longer, then by sudden onset of black shale sedimentation dur­ ing the G. persculptus Zone or Parakidograptus acuminatus Zone . A distinctive shelly fossil assem­ blage termed the Hirnantia fauna is found within many of these late Ordovician marine deposits . It is diachronous, probably ranging in age from the Dicellograptus anceps Zone (D. complexus Subzone) to the G. persculptus Zone, and has been considered to represent a cold water fauna related to the late Ordovician glaciation . Such conclusions have, how­ ever, been questioned (Rong in Bruton 1984) . In addition to the eustatic changes, a major palaeobio­ logical event occurred during the Late Ordovician; this is one of the four largest mass extinctions during the Phanerozoic (Section 2 . 13.2) .

5 . 10 . 3 Ordovician - Silurian C . R . BARNES & S . H . WILLIAMS

Historical background The Ordovician System was introduced by C . Lapworth in 1879, in a successful attempt to solve the mid-nineteenth century acrimonious debate begun by A. Sedgwick and R. Murchison . Lapworth

Ordovician - Silurian Boundary Working Group In 1976, the Ordovician- Silurian Boundary Work­ ing Group of the lUGS Commission on Stratigraphy (Section 5 .8) was created to formally define the stratigraphic level and boundary stratotype location for the base of the Silurian System . Over the sub­ sequent eight years it received over 50 reports from geologists around the world and organized major field excursions . The criteria which ideally should

479

5. 1 0 Global Boundary Stratotypes

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be met by boundary stratotypes are set out i n Sec­ tion 5 . 1 0 . 1 . The task of the Working Group proved unexpectedly difficult as sections became subjected to intense research . In most localities thought to approach the ideal criteria, one or more stratigraphic breaks occurred (e . g . disconformity, barren interval, or regional regression) and they were therefore deemed inadequate for stratotype status. The recognition that a low sea-level stand near the boundary exposed many regions of earlier deposi­ tion forced the Working Group to focus on sections representing marginal basins (e . g . Anticosti Island, eastern Canada) or deep oceanic settings (e . g . Dob's Linn, southern Scotland) . These were contrasting sections in many of their attributes, and neither provided a perfect candidate for the boundary stratotype . Anticosti Island in the Gulf o f St. Lawrence, Quebec, preserves a 1500 m stratigraphic section of late Ordovician -early Silurian age . Limestones and minor shales predominate and represent de­ position within a low latitude marginal basin .

The strata are accessible, well exposed, scarcely deformed or thermally altered, and yield prolific, well preserved fossils (Barnes 1988) . Graptolites are rare, but biostratigraphic control is possible with several other fossil groups, of which conodonts are the best studied . McCracken & Barnes (1981) pro­ posed a system boundary 0 . 9 m above the base of member 7 of the Ellis Bay Formation at Baie Ellis, based on the first appearance of Ozarkodina oldhamensis . The section possesses most of the characteristics required for a stratotype, but lacks sufficient graptolites to provide good correlation into oceanic facies . Dob's Linn lies within the Southern Uplands of Scotland, northeast of Moffat. The Moffat Shale Group comprises over 100 m of black, grey and siliceous shale and is divided into four forma­ tions ranging from the Nemagraptus gracilis Zone (Llandeilo) to the Rastrites maxim us Zone (Lland­ overy) . With the exception of the Upper Hartfell Shale Formation, most of the Moffat Shale is con­ tinuously graptolitic and has been renowned for its

480

5 Taxonomy, Phylogeny, and Biostratigraphy

rich, diverse fauna since Lapworth published his landmark study in 1878 . Other fossil groups are, however, mainly absent, with the exception of rare deep-water trilobites, brachiopods, and conodonts . The late Ordovician and early Silurian succession at Dob' s Linn has recently been subjected to critical, systematic study (see Williams 1988) . Although most of the Upper Hartfell Shale is composed of grey, non-graptolitic mudstones, occasional graptolitic black shale bands occur. Of particular importance to the Ordovician - Silurian boundary are the Anceps Bands and Extraordinarius Band (Fig . 1) . The Anceps Bands yield a rich, diverse fauna; in con­ trast, the following Extraordinarius Band contains only three graptolite taxa, as does the lowest part of the Birkhill Shale belonging to the G. persculptus Zone . During this and the succeeding P. acuminatus Zone, new taxa appear to give a more diverse, typically Silurian assemblage . The Ordovician ­ Silurian boundary was historically considered to lie at the boundary between the Upper Hartfell and Birkhill Shale; the Working Group, however, con­ sidered this to be an unsuitable horizon at which to place the boundary, owing to unfossiliferous strata and the lack of major faunal change . The boundary was consequently defined at the base of the P. acuminatus Zone, 1 . 6 m above the base of the Birkhill Shale . It is recognized by the first occurrence of Akidograptus ascensus and P. acuminatus, an event which may be accurately correlated in many sections throughout the world . The final recommendation of the Working Group, with Dob' s Linn as stratotype, was approved by the lUGS in 1984 . Some concerns about the decision were expressed by Lesperance et al. (1987) .

References Barnes, c . R . 1988 . Stratigraphy and palaeontology of the Ordovician - Silurian boundary interval, Anticosti Island, Quebec, Canada. Bulletin of the British Museum (Natural History) Geology Series 43, 195 - 219. Bruton, D.L. (ed . ) 1984. Aspects of the Ordovician System . Paleontological Contributions from the University of Oslo, No. 295. Universitetsforlaget, Oslo . Lapworth, C. 1878 . The Moffat Series . Quarterly Journal of the Geological Society of London 34, 240- 346. Lapworth, C . 1879 . On the tripartite classification of the Lower Palaeozoic rocks . Geological Magazine (Decade 2) 6, 1 - 15 . Lesperance, P . J . , Barnes, C . R . , Berry, W . B . N . , Boucot, A.J. & Mu Enzhi. 1987. The Ordovician- Silurian boundary stratotype : consequences of its approval by lUGS . Lethaia 20, 217-222.

McCracken, A.D. & Barnes, C . R . 1981 . Conodont biostra­ tigraphy and paleoecology of the Ellis Bay Formation, Anticosti Island, Quebec, with special reference to late Ordovician -early Silurian chronostratigraphy and the systemic boundary. Bulletin of the Geological Survey of Canada 329, 51 - 134. Williams, S . H . 1988. Dob's Linn, the Ordovician- Silurian boundary stratotype . Bulletin of the British Museum (Natural History) Geology Series 43, 17-30 .

5 . 10 . 4 Silurian - Devonian C . H . HOLLAND

The standardization o f the Silurian - Devonian boundary can be taken as a case history in inter­ national stratigraphic procedure . As the first such boundary to be agreed in modern fashion, some have regarded it as a kind of model . Others see the period of more than 12 years involved in settling the matter as being something of a warning. The main problem, causing this long gestation, was that of the 'lost series' (now referred to as the Pndoli) a series lost in previous erroneous correlations .

Historical background In 1834 R. Murchison showed the Tilestones of south Wales to be the basal part of the Old Red Sand­ stone . Later he moved the basal boundary to the top of the Tilestones, perhaps because by then he re­ garded their lower part as corresponding to the Downton Castle Sandstone of Shropshire, which he had previously taken as the top of his Upper Ludlow Rock. There is no available section crossing from the marine Devonian rocks in their type area of Devon into the Silurian System in its type area in the Welsh borderland . The different positions of the boundary accepted by various subsequent authors through the years have been documented by White (1950) . White chose the base of the Ludlow Bone Bed as the base of the Old Red Sandstone, making for the sake of practicality the 'slight adjustment' necessary beyond the boundary originally designated by Murchison . Later workers in the Welsh borderland were grateful for the stability thus achieved . In their revision of the Ludlow Series in its type area,

481

5 . 1 0 Global Boundary Stratotypes Holland et al. (1963) designated a standard section for the base of the Ludlow Bone Bed at 'Ludford corner' in the town of Ludlow, Shropshire . In the meantime, Martinsson was achieving success in the use of ostracodes to correlate the Welsh borderland succession into the Baltic region and beyond, and Boucot was beginning to recognize the presence in such areas as Podolia (Ukraine, U . 5 . 5 . R. ) of a brachiopod fauna which appeared to fall between that of the Ludlow Series and that of the Gedinnian in Belgium.

rapidly changed, much new work was initiated, and the Committee on the Silurian -Devonian Boundary began its 12 years of work. Because of the previously erroneous correlation, the choice of a horizon for the boundary had to come first and it was inevitable that this would involve a measure of compromise (Fig. lA) . A level at the base of the Monograptus uniformis Biozone was first suggested by Holland (1965) and received early support in a paper by Czech colleagues . This horizon was eventually accepted by the Committee . At this time, the Committee also developed a set of criteria which it judged to be important in the subsequent selection of a location for the boundary stratotype . These included level of faunal and floral development, stratigraphic considerations, structural situation, facies diversity, geographical accessibility, and the possibility of conservation of the section. After many submissions had been received and members of the Committee had undertaken a variety of field visits, a short-list of four candidates emerged for the boundary stratotype : Morocco; Nevada, U . 5 . A . ; Podolia, Ukraine, U . 5 . S .R. ; and Bohemia, Czecho­ slovakia. In the desert country on the edge of the Sahara in southwest Morocco, the Silurian-Devonian Bound­ ary can be located near the small oasis of Ain Deliouine . It is difficult of access, but the factor most weighing against this section was the serious effect of desert weathering upon the graptolites

Committee on the Silurian-Devonian Boundary In Central Europe, however, research workers, building upon the monumental work of Barrande, were becoming increasingly disillusioned with a Silurian -Devonian boundary that they found con­ sirably difficult to use in correlation . They needed a succession in fully marine facies . At a meeting in Prague in 1958 Czech stages were formalized, but much more was achieved at the epic Bonn -Brussels meeting of 1960 organized by H.K. Erben. There was one particular discussion (at the back of a coach) during this meeting when everything became clear. Suddenly there was the realization that the graptolites did not disappear in some mystical way at the end of Silurian time but continued into the Devonian . After the meeting, correlation tables were

A

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WELSH B O R D E R LA N D

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S I LU R I AN

Prid o l f Fig. 1 A, The compromise in­ volved in establishing inter­ national agreement on the placing of the Silurian- Devonian Boundary. (After Holland 1986 . ) B, Boundary stratotype for the base of the Devonian System at Klonk, Prague Basin, Czechoslovakia. (After Chlupac et a/. 1972 . )

Lud low bone bed

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482

5 Taxonomy, Phylogeny, and Biostratigraphy

close to the boundary . In Nevada, the basin and range country provides good Silurian - Devonian sections . In spite of the tectonic isolation of the ranges, individual " sections (such as those in the Roberts Mountains) are clear. It is important, how­ ever, that decisions on stratigraphic standardi­ zation should be achieved with reasonable expedition, and work in Nevada was insufficiently advanced . Podolia in the Ukraine is a magnificent area for Silurian - Devonian geology, with highly fossiliferous strata exposed in structurally simple sections along kilometre after kilometre of the Dnestr River and its tributaries . Unfortunately, no graptolites had been found in the beds immedi­ ately below the chosen horizon and there were also some problems of access. So Barrande's classic area in the Prague basin (Barrandian area) was chosen for the stratotype (Chlupac et al. 1972), backed by extensive collections in the National Museum, Prague . The section at Klonk (Fig . 18) was preferred to the structurally more complex alternative at Karlstejn; the 'golden spike' was placed at the point where Monograptus uniformis first appears within 'Bed 20' . This final decision was ratified at the International Geological Congress in Montreal in 1972, when the Committee on the Silurian -Devonian Boundary

reported through the Chairman, D. J. McLaren, to its parent body, the International Commission on Stratigraphy (Section 5 . 8), and thence to the Inter­ national Union of Geological Sciences (Martinsson 1977) . Since then the choice of horizon has proved significant, allowing for sensible correlation tables in which the Piidoli Series plays its part as the fourth series of the Silurian System.

References

Chlupac, L, Jaeger, H. & Zikmundova, J. 1972. The Silurian ­ Devonian Boundary in the Barrandian . Bulletin of Canadian Petroleum Geology 20, 104 - 1 74. Holland, CH. 1965 . The Siluro-Devonian Boundary . Geological Magazine 102, 213-22l . Holland, CH. 1986. Does the golden spike still glitter? Journal of the Geological Society 143, 3-2l . Holland , C H . , Lawson, J.D. & Walmsley, V.G. 1963 . The Silurian rocks of the Ludlow district, Shropshire . Bulletin of the British Museum (Natural History) Geology Series 8, 93 - 1 7l . Martinsson, A . (ed . ) 1977. The Silurian - Devonian Boundary. International Union of Geological Sciences, Series A, No . 5. E . Schweizerbart'sche Verlagsbuchhandlung, Stuttgart. White, E J . 1950 . The vertebrate faunas of the Lower Old Red Sandstone of the Welsh borders. Bulletin of the British Museum (Natural History) Geology Series 1, 49- 67.

5 . 11 Fossils and Tectonics R . A . F O RT E Y & L . R . M . C O C K S

Introduction The history of palaeontology has been closely con­ nected with contemporary developments in other branches of the earth sciences . Until 30 years ago the subdisciplines of geology were less clearly separated than they are now, and the all-round geologist might routinely use fossils as part of his armoury of field data in unscrambling the prob­ lems of a structurally complex area. Fossils had an immediate part to play in resolving tectonic prob­ lems, and the structural geologist would use them at an early stage in the generation of his hypoth­ eses; conversely, many invertebrate palaeontol­ ogists would not feel abashed at concocting

structural hypotheses of their own . In the U.K. this was particularly true of Lower Palaeozoic studies, and it would not be overstating the case to say that palaeontology made as much of a contribution to working out the structure of Wales as any other geological discipline . In the nineteenth century the great works of Murchison and Sedgwick carried their palaeontological notes and appendices (e . g . Murchison 1839), and i t i s obvious that these authors used the fossils as guides and friends to find their way through these 'interminable greywackes' . Nowadays there are few great generalists of this kind - the sheer proliferation of techniques and knowledge has made it impossible . As a conse­ quence, tectonics, geochemistry, and sedimentology

5. 1 1 Fossils and Tectonics have separated as independent disciplines, and theories of structural intent may come from any one of them . Palaeontology is too often neglected entirely - but this is to miss evidence of practical usefulness . Conversely, the number of palaeontol­ ogists with an eye for structural problems has also diminished, partly because of the growth in the palaeobiological side of the subject, and partly because of the increasing specialization which is characteristic of all science . Fossils do, however, still have an important part to play in the testing of tectonic theories in parts of the world where metamorphism has not destroyed the evidence entirely - and even in global prob­ lems. Perhaps the best way to regard fossils in a tectonic context, and the role of palaeontology as a separate discipline, is as a critical test of theories generated from any of the other geological sub­ disciplines; conversely, theories derived from palaeontological evidence must themselves pass muster with the tectonicist, the geochemist, or the sedimentologist . No matter how a theory is orig­ inally derived, it becomes plausible only when supported by different lines of evidence from several disciplines . The unique contribution of palaeontological evidence is that it does not depend directly or covertly on other sources of evidence; circular arguments are always hard to avoid in geology, and fossils can cast a hard factual light on tectonic speculation .

Classical uses of fossils in tectonic problems The most basic use of fossils, especially inver­ tebrates, is in the dating of rocks . In spite of the tremendous advances in radiometric geochronology there is no substitute for a reliable palaeontological age, because, unlike radiometric 'clocks', fossils cannot be 'reset' by later events (see also Section 5 . 1 0 . 1 ) . Limitations are only set by the recognition of the fossils themselves - but occasionally these can be powerful limitations if the rocks that contain them have been heavily cleaved, distorted, or meta­ morphosed . Even so, it is surprising how much punishment fossils can endure before they are completely obliterated . For example, in the Appalachians Silurian brachiopods have survived sillimanite grade metamorphism to date a huge tract of otherwise barren metamorphics (Boucot & Thompson 1963); in the Alps belemnites are still recognizable after enduring extreme tectonization . Generally, fossils in shales are severely affected before those in limestones or sandstones . Even such

483

distortions have their uses, if the original dimen­ sions of the fossil are known, because they can provide a measure of extension or compression and thereby permit the calculation of the strain ellipsoid affecting the enclosing rocks . The classical uses of palaeontological dates in tectonics can be summarized in three categories : 1

The dating of phases of movement or igneous/meta­ morphic activity from unconformities . An uncon­

formity between two sedimentary formations can provide a close control on the age of movement, which is after the youngest fauna or flora found below the unconformity and prior to the oldest fauna found above it . This can provide a very precise control, as in the famous Bala unconformity in the Ordovician of north Wales where there is a gap between the Middle Caradoc and the Middle Ashgill . Dates for phases of intrusion or metamor­ phism are only 'older than' the age of the earliest overlying sediment and need supplementary evi­ dence from radiometric dating .

2 The determination of facing direction or 'way up' in folded areas . In geologically complex country the

younging direction of beds is frequently obscure, especially where the rocks are monotonous in lith­ ology . Fossils often provide the only means of un­ scrambling such successions . The classic example is C. Lapworth's interpretation of the Southern Uplands of Scotland, which ran in tandem with the same author' s identification of the sequence of graptolite faunas . Lapworth made sense of a hitherto un­ interpretable stretch of country, comprising appar­ ently endless shales . It is only recently that Lapworth's structural interpretation has been revised; even now, his palaeontological evidence stands almost intact . 3 Dating volcanic activity. Submarine or sub aerial volcanics are often interbedded with fossiliferous rocks, and have long been dated thereby . Volcanics play an important part in the history of active continental margins. More recent work on the geo­ chemistry of such rocks is able to identify the palaeogeographical setting precisely (such as whether they are island arc or back arc volcanics) . With fossils to provide the chronology, the tectonic and volcanic history can now be detailed more informatively than in the days before plate tectonic modelling. Such an approach has profoundly altered our understanding of marginal basins, such as the Caledonian Welsh basin (Kokelaar & Howells 1984) . A few kinds of fossils - graptolites and radiolaria especially - can even be found in the sediments

484

5 Taxonomy, Phylogeny, and Biostratigraphy

associated with ocean-floor basalts . These provide the only non-radiometric evidence for the date of eruption of ocean-floor magma, and for the sub­ sequent obduction of volcanics . Such applications rely on fossils as tools for dating rocks, without necessary regard to the palaeo­ biology, palaeoecology, or distribution of the organ­ isms concerned . Although such uses have a long tradition, they are as appropriate today as they ever were . For those with the patience to search tec­ tonized areas new faunas still turn up; and when they do, the implications can be important. For example, unpromising-Iooking limestones in the Highland Border Complex of Scotland have recently yielded Ordovician silicified faunas (Curry et al. 1984) which not only rule out at least one previous tectonic interpretation, but also suggest the presence of former Ordovician basins in the area now occu­ pied by the Midland Valley . Other recent appli­ cations of fossils in tectonics draw on the whole range of properties of fossil assemblages as well as their capacity to date rocks . These are considered next.

Nappe tectonics Nappes are the characteristic feature of the Alpine style of deformation, in which great, dislocated folds are translated horizontally - in some cases many kilometres from their original 'root zone' . Nappe may pile on nappe, often with the highest nappe being the one that has travelled furthest. Such scrambled geology often resists interpretation . Fossils can contribute in several ways to unravelling these complexities : (1) they can date each nappe 'package', which often has a discrete stratigraphy when compared with its neighbours; and (2) the kind of facies and faunal assemblages can often contribute to locating the site from which the nappe has travelled, or help towards the reconstruction of the original palaeogeography. It is only unfortunate that nappe country is often also metamorphosed, removing fossil evidence . Even so interpretation can proceed on occasion by extrapolation from ad­ jacent, less metamorphosed areas. The interpretation of the Swedish Caledonides in terms of nappe tectonics is a relatively recent inno­ vation; faunal evidence is sporadic, but has made a vital contribution to unravelling the complex tec­ tonics in the upper allochthon of the Trondheim region (Gee & Roberts 1983) . In a generally anal­ ogous way the somewhat monotonous tract of domi-

nantly clastic Upper Palaeozoic rocks of southwest England is now being reinterpreted as a nappe complex. Fossils (especially conodonts and goniatites where these occur) supply valuable fixed points in this shifting stratigraphy. In the continu­ ation of the Alpine belt eastwards into the complex regions of Timor, where arcs have appeared, dis­ appeared, and collided, the microfossil stratigraphy (especially using foraminifera) has proved the key to unlocking the late Tertiary structural history (e . g . Audley-Charles 1 986) . In such areas the struc­ tural geologist and the palaeontologist work closely together, to their mutual benefit.

Palaeobiogeography and tectonics Fossil taxa, unless they are unique examples, have a spatial distribution which can be used to construct palaeobiogeographical maps . For post-Palaeozoic distributions these maps can be tested against con­ tinental reconstructions derived from geophysical data, but nowadays the fossils themselves are not often used as the basis of reconstructing past geo­ graphy, although they were very much part of the argument about Pangaea in the twenties and thirties (see also Section 6 . 5 . 2) . In the earlier Palaeozoic, however, geophysical data are sparse and ambigu­ ous, and the continental configurations were dif­ ferent both from Pangaea and from the present; here fossil distributions can still contribute to hypotheses about the disposition of ancient continents . Such continents were, of course, separated by oceans as they are today - but oceans that have long since vanished. The proof of their former existence is tectonic, in that the disappearance of an ocean by subduction leaves a unmistakable tectonic imprint . But former oceans also influenced palaeobiogeogra­ phy. Oceanic separation tends to induce endemicity in the seas surrounding separated continents especially among shallow-water organisms - and particularly if oceanic separation is accompanied by latitudinal separation and hence a climatic barrier. The former existence of such an ocean can then be recognized by the close apposition today of two large areas with their own endemic shallow­ water faunas . Between such areas there should be a 'mobile belt' with its own faunal peculiarities, as we describe below. These palaeobiogeographical differences should not be attributable to some other physical factors, such as salinity or substrate . Once the possibility of the existence of a former ocean is identified using fossils, the tectonicist and geochemist may search for the other signatures that

5 . 1 1 Fossils and Tectonics a vanished ocean leaves in the folded rocks . One example concerns the Ordovician history of the British Isles. It has long been recognized that the early Ordovician rocks of northwest Scotland were very different from those of Wales and the Lake District, and contained different faunas . Recent plate tectonic interpretations explained such differences by postulating the existence of a former ocean - a 'proto-Atlantic' or Iapetus . The destruction of this ocean at the end of the Lower Palaeozoic resulted in the Caledonian mountain belt, which extends both soutwards into the Appalachians and northwards all along the western coast of Scandinavia. North­ west Scotland (indeed Scotland as far south as the Southern Uplands) belonged to the North American side of Iapetus, which explained both the faunal differences and the tectonics . The continent at the other side of the ocean was regarded as comprising the Anglo-Welsh area (together with the rest of Southern Europe) as well as Baltica. However, faunal studies showed great differences between the shallow-water trilobite and brachiopod faunas of Southern Europe, including England and Wales, and those of the Baltic platform. These areas ap­ proach one another closely today, and it is not possible to explain away these differences simply as a geographical cline . Cocks & Fortey (1982) showed that the differences in the Early Ordovician were consistent with climatic separation: Laurentia (and Scotland) was tropical; Baltica was probably at tem­ perate latitudes; while the Anglo-Welsh area was likely to have been at high palaeolatitudes as part of an Ordovician Gondwana (Fig. 1 ) . An oceanic tract, called Tornquist's Sea, was considered to have separated Baltica from the Anglo-Welsh area. Since this ocean subsequently closed, the region of closure should have the appropriate tectonic style . Geological investigations being carried out at the moment seem to confirm the idea of a vanished Tornquist's Sea. This is a case where a knowledge of fossils has led directly to new tectonic interpret­ ations . Such methods do depend on the actualistic assumption that climatic zones controlled the dis­ tribution of fossil taxa in the same way as they control the distribution of the living biota . The fact that other, independent geological evidence seems to confirm the conclusions drawn from fossils vin­ dicates these methodological assumptions .

Biofacies and tectonics Recent marine environments are diverse and pro­ vide different habitats for animals and plants ac-

485

cording to such factors as substrate type, water depth, temperature, oxygen saturation, and so on . Communities of benthic organisms tend to 'club together' in appropriate environments, even though many such communities intergrade in complex ways . There is no reason to suppose that fossil faunas were any different, although identification of fossil 'communities' is hampered by the partiality of the fossil record . None the less it is common to find constant associations of fossil taxa (usually genera) associated with particular palaeoenviron­ ments . Sometimes these generic associations persist for tens of millions of years . Many different terms have been applied to describe such associations communities, community types, constant generic associations (CGAs), for example - but the one in commonest currency is biofacies, the palaeo­ biological equivalent of the sedimentary lithofacies (Sections 4 . 1 7, 4 .18) . Biofacies can be important aids in tectonic prob­ lems . Some of the more important biofacies are related to the depth - temperature profile running from shallow-water epicontinental to deep-water oceanic. As we have seen, the shallow-water faunas may lead us to conclusions about palaeoclimatic distribution of faunas - and hence to conclusions about the presence of ancient oceans . In a com­ plementary way, the more exterior, ocean-facing biofacies may afford a method of charting the edges of former oceans, or at least deep marginal basins . Such marginal biofacies should be found along putative sites of former subduction . However, the deeper biofacies do not provide a ready method of saying which side of an ocean a fauna occurred, because one of the properties of exterior biofacies is that they are less tied to one particular continent some genera may, indeed, be pandemic . An example from the Ordovician, contemporaneous with Iapetus (above), is the distribution of the graptolite isograptid biofacies . Even at the same time as the epicontinental faunas were divided into separate endemic faunas, corresponding with the distri­ bution of continents and climatic belts, the isograptid biofacies is found worldwide, but its distribution corresponds very closely with the mar­ gins of the proposed continents (Fig . 2) . This means that the discovery and mapping of sites containing the isograptid faunas can contribute to the under­ standing of global tectonics : since such a biofacies can be readily identified, even from small fragments (Fortey & Cocks 1 986), it can afford valuable clues to the former existence of deep basins in advance of detailed geological mapping.

486

5 Taxonomy, Phylogeny, and Biostratigraphy

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Where continents converge during phases of sub­ duction, the normal sequence of biofacies may become tectonically reshuffled. This may allow some estimate of the horizontal and vertical displace­ ment involved during earth movements . In the Cambrian - Ordovician Cow Head Group of western Newfoundland (James & Stevens 1986), autochthonous shales accumulated off the edge of the North American shelf, and were augmented by gravity slides of boulders derived from shallower biofacies . Fossils from these boulders show that the gravity slides included samples from deep shelf environments, originally at several hundred metres water depth, as well as typical shelf limestones . Subsequently, the whole Cow Head Group has been thrust onto the platform - moving deep­ water biofacies onto shallow-water biofacies in the process .

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Independent proof for suspect terranes Suspect terranes are pieces of crust of less than continental size, the original position of which is in dispute; some have become detached and displaced, even for many hundreds of kilometres . It is obvious, from such major tectonic movements as the San Andreas Fault in western North America today, that relative displacement of terranes can occur quite quickly. However, in analysing fossil distributions which can indicate such terrane movement in the past, it is essential to be sure that the correct comparisons are made between relevant fossils of the same age and biofacies . It is much easier to differentiate movements north - south across lati­ tudes by palaeontological methods, since tempera­ ture plays such an important role in controlling the distribution of many fossils, than east- west across

5. 1 1 Fossils and Tectonics

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longitudes, where significant terrane movement can occur without appreciable change in the faunas . For example, an analysis of fusuline foraminifera of Permian age along the western North America belt

reveals that verbeekinid fusulines, which are charac­ teristic of the Eurasian Tethys, are confined to a fault-bounded area, the Cache Creek Terrane of British Columbia; in contrast, the surrounding areas

488

5 Taxonomy, Phylogeny, and Biostratigraphy

have fusulines of non-Tethyan, North American cratonic aspect (Monger & Ross 1971 ) . Such work has led to the recognition of nine separate allo­ chthonous terranes along the Pacific seaboard, some of which appear to have been as far away as Japan in Permian times (Fig . 3) . Some longitudinal dis­ placements may be detected when discrete faunal provinces that were originally separated, perhaps by a major oceanic barrier, subsequently become juxtaposed after terrane movement; but this can be recognized only when differing faunas are dis­ placed towards one another, as opposed to tracking the east- west path of a terrane diverging away from its parent palaeocontinent.

Tectonic uses of sea-level curves By assessing the distribution of benthic fossils in a basin at a single geological period, shallow- to deep­ water assemblages may be recognized, with diver­ sity (number of different species) increasing away from the shore . From these distributions a qualitat­ ive assessment of water depth (at least from shore­ face, shallow shelf, mid-shelf, deep shelf, to oceanic assemblages) may be made (see also Section 4 . 19.5) . By plotting and comparing these relative palaeo­ depths from one area over a succession of geological ages, a graph may be drawn up of changing depths with time, known as a sea-level curve. Whilst such curves are relatively objective, their interpretation requires more thought, since the change of sea-level at one place can be caused either by the rise and fall of the sea itself (eustatic changes), or by the rise and fall of the ocean floor (tectonic changes), or by a combination of the two . However, if the migration of biofacies indicating a transgression or regression is paralleled at exactly the same time in several tectonically independent palaeocontinents, then it is fairly certain that the sea-level changes were eustatic (Fig . 4) . For example, sea-level changes appear to have been at their highest during the Cretaceous (Cenomanian) and Ordovician (Caradoc), which explains the wide-spread transgressive sequences recorded from those times, and at their lowest during such events as the late Ordovician and late Permian glacial intervals, when substantial amounts of water must have been locked up as polar ice . When sea-level curves are anomalous and move in different ways in different places, then tectonic control is indicated . Fig . 5 shows an analysis of sea­ level curves for Wales during an extended interval of nearly 70 Ma in the Ordovician and Early Silurian,

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as compared with the global eustatic sea-level curve (Fortey & Cocks 1 986) . The separate curves for north Wales and south Wales parallel the global curve for much of the period, but in the Late Arenig, Llandeilo, and Late Caradoc the north Welsh curve is much displaced from the global curve and dis­ placement occurs in the south Wales curve at the

489

5. 1 1 Fossils and Tectonics Lago o n s w i t h evapo r i t e s , gastropod s , s t ro m ato l ites etc.

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were derived) . Note how the local eustatic curves follow the global curve except when they are modified by nearby tectonic activity. (From Fortey & Cocks 1986.)

490

5 Taxonomy, Phylogeny, and Biostratigraphy

same (late Caradoc) time . These discrepancies re­ veal not only periods of contemporary tectonic unrest, but how far-reaching any particular tec­ tonic disturbance was . It is interesting to note, for example, that the sea-level curve is affected by the late Llandeilo vulcanicity in north Wales, which includes the volcanic outpourings of what are today Snowdon and other mountains, whilst the contem­ porary curve for south Wales, only 120 km to the southwest, appears to have been closer to the global curve . This indicates that, assuming an Ordovician geographical separation of the two areas similar to that seen today (which seems likely), the volcanic tectonicity in north Wales was relatively restricted in area.

References Audley-Charles, M . G . 1986. Rates of Neogene and Quaternary tectonic movements in the Southern Banda Arc based on micropalaeontology. Journal of the Geological Society 143, 161 - 1 75 . Boucot, A.J. & Thompson, J . B . 1963 . Metamorphosed Silurian brachiopods from New Hampshire. Bulletin of the Geologi­ cal Society of America 74, 1313- 1334. Cocks, L .R.M. & Fortey, R.A. 1982. Faunal evidence for oceanic separations in the Palaeozoic of Britain. Journal of the Geological Society 139, 465 -478 .

Curry, G . B . , Bluck, B.J., Burton, c .J . , Ingham, J . K . , Siveter, D.J. & Williams, A. 1984. Age, evolution and tectonic history of the Highland Border Complex, Scotland . Trans­ actions of the Royal Society of Edinburgh (Earth Sciences) 75, 113- 133. Fortey, R.A. & Cocks, L . R . M . 1986. Marginal faunal belts and their structural implications, with examples from the Lower Palaeozoic. Journal of the Geological Society 143, 151 - 160 . Fortey, R . A . & Cocks, L . R . M . 1988. Arenig t o Llandovery faunal distributions in the Caledonides of the North Atlantic Region. Special Publication of the Geological Society No. 36 . Gee, D . G . & Roberts, D. 1983 . Timing of deformation in the Scandinavian Caledonides . In: P . E . Schenk (ed . ) Regional trends in the geology of the Appalachian - Caledonian ­ Hercynian-Mauritanide- Orogen, pp. 279- 292. Reidel, Dordrecht. Hallam, A. 1986. Evidence of displaced terranes from Permian to Jurassic faunas around the Pacific margins . Journal of the Geological Society 143, 209-216. James, N . P . & Stevens, R.K. 1986. Stratigraphy and corre­ lation of the Cambro-Ordovician Cow Head Group, Western Newfoundland . Bulletin of the Geological Survey of Canada 366, 1 - 143 . Kokelaar, B . P . & Howells, M.F. (eds) 1984. Marginal basin geology. Special Publication of the Geological Society No . 16. Monger, J.W.H. & Ross, C . A . 1971 . Distribution of fusuli­ naceans in the western Canadian Cordillera. Canadian Journal of Earth Sciences 8, 259- 278. Murchison, R . I . 1839 . The Silurian System. John Murray, London.

6

INFRA S T RUCTURE

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6 . 1 Computer Applications in Palaeontology J . A . KITCHELL

Introduction

that are made into models use the explicit language of mathematics . The purpose of mathematical modelling is to capture in specific and explicit terms the essential bits and connections of the theory. The purpose of simulation modelling is to take this process a step further: simulation is an exploratory technique . Simulation modelling explores the consequences of a given set of assumptions . The outcome is created as a logical consequence of the theorized process, to discover the way things would be, if the theory of process were operative . Using the capability of the computer the technique is used to determine whether, given a certain formulation of a process or system, this formulation (i. e . this set of assump­ tions) can produce behaviour similar to that known empirically . Such an approach is necessary to aug­ ment and even to develop our limited intuition in dealing with complexity (e . g . solving simultaneous situations) and nonlinearity . Modelling becomes indispensable when it expands the limits of our understanding beyond both intuition and the ex­ ploration of what did happen to what could happen . Another important aspect of the computer has been referred to as 'its power to feed a new math­ ematics of the eye' (Gleick 1987) . What this means is that images (easily readable graphic output) have increasingly replaced more abstract formu­ lations . Such graphics are also necessitated by the fact that there is no unique solution to many the­ ories (models) . The dynamics and range of solutions can now be shown in the form of a 'portfolio' (Fig . 1 ) . Most of the work in palaeontology using simulation modelling has relied on this appeal of graphic imagery. Examples include the behaviours of random processes, the transformation of mor­ phologies, and the features of time series . In palaeontology, simulation modelling has been used largely in the following cases : (1) to model aspects of randomness, as a branching process, a diffusion process, or a random walk; (2) to model growth and form and the (descriptive) transform­ ation of related morphologies; and (3) to model the behaviour of classical functions (e . g . the exponential and logistic) . In each of these cases (except the

Computer techniques enable palaeontological questions to be addressed on a scale unheard of in earlier times . The capacity of the computer to organize and manipulate immense amounts of information is well known. Consequently, this article is not about computer applications that merely change the magnitude of analyses but is instead a response to the question 'What qualitative changes have resulted from this quantitative leap in com­ puting speed, efficiency, and capability?' The focus will be on 'the new eyes' provided by the computer, emphasizing the ways in which computing tech­ niques enhance our ability to 'see' both problems and data.

The computer as experimental tool True experiments are not possible within the his­ torical sciences, because history cannot be repeated in novel contexts . Computer modelling serves in­ stead as the experimental tool . Experimentation is made possible by the fact that simulation models, unlike analytical models, have no exact solution . Evolutionary theory and simulation modelling are in this respect analogous . Each simulation run may represent a different evolutionary trial in which differences and novel contexts are introduced by stochastic variables or changing parameter values of deterministic variables . By explicit and systematic manipulations, the palaeontologist is given the power to complete 'If . . . then . ' statements about evolutionary process and the resultant pattern . Despite the fact that 'scientists are incessantly saying to each other "Let's play around with that" and modelling is the quintessential way of playing with the way things might work and might be' (Judson 1980), palaeontologists historically have not developed mathematical models . Yet it is well understood that theories, whether explicitly or implicitly, are mathematical, even though the impetus of theory formulation is outside mathemat­ ics and distinctly empirical . As a result, theories .

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The approach that yielded these results combines simulation modelling with a statistical analysis dependent on computer solution. The research question requires that the expected distributions of temporal covariation among clades generated by a random process be known . Because there is no analytical solution to the problem, a random branching process was used to generate 45 000 simulated monophyletic clades, where the differences between each clade's history are due to the random elements of the branching algorithm. Each evolutionary 'trial' of 90 such clades, allowed to evolve for 63 time steps (where 90 and 63 were chosen to match the empirical data of number of taxa and stratigraphic stages, respectively), was then subjected to Q-mode factor analysis (to match the method of analysis of the empirical data) . The frequency distribution of these 500 factor analyses are shown in A, C, and E which represent Factors I, II, and Ill, respectively. The stippled areas of B, D, and F represent the corresponding patterns not significantly different from expectations of a random branching process. (After Kitchell and MacLeod 1988 . )

coupled logistic) the exploration of behaviour involves only kinetics . Kinetics are more inherently intuitive than dynamics, which incorporates feedback. A more ambitious undertaking of theory develop­ ment and simulation exploration involving feed­ back, nonlinearity, and complexity, is the work of DeAngelis et al. (1985) on potential coevolutionary dynamics, a series of studies motivated by (but not confined to) palaeontological questions . What this work has gained is a new intuition to replace the old expectation of linear escalation . In addition, it

has shown the salient features of nonlinear dynam­ ics (Fig. 2) : how the behaviour of the individual parts are qualitatively different from the behaviour of the whole; and the influence of evolutionary change on itself, where 'playing the game changes the rules' . Computer-intensive statistical inference

Science is argument focused on the differential credibility of competing hypotheses . Palaeontology, a historical science, must make argument of process

6 . 1 Computer Applications in Palaeontology (where the interest generally lies) from evidence of pattern (where the information generally lies) . Fortunately, hypotheses of process contain predic­ tions of pattern, and so there can be effective argu­ ment provided by historical pattern. Statistics similarly deals with an end product (namely, some observed set of data) and makes arguments, among others, regarding what factors are, and to what extent, causally responsible . The power of computing is currently changing the field of statistics . In general, the computer has allowed even classical statistical methods to be applied to what would once have been unmanage­ ably large data sets . Palaeontology has benefited from this increased capability; the compilation and analyses of large databases have changed the tenor of arguments, for example, on patterns of diversifi­ cation (Section 2 . 7), extinction (Section 2 . 12 . 3 ), rates of phenotypic evolution, and taxonomic turnover (Section 2 . 1 1 ) . Palaeontology, however, has been hampered by the limits of classical statistics : the need to make a priori assumptions about the form of the probability distributions that are sampled by the data, and the restriction to measures whose theoretical properties are simple enough to have analytical proofs . These limits have been trans­ cended recently by computer recursion techniques that replace analytical solutions with enormous numbers (105 - 10 9 ) of computations . Boots trapping represents such a computer­ intensive method, described as the 'substitution of raw computing power for theoretical analysis' (Efron & Gong 1983) . Using the traditional approach, one would hypothesize a process (or model) and deduce (or simulate) its behaviour, to compare these outcomes with empirical data . The boots trapping approach is logically different. Bootstrapping derives its power from the assumption that the empirical sample provides an informative 'glimpse' of the real or underlying process. This empirical sample is resampled with replacement a large number of times, with the statistic(s) of interest calculated for each boots trapped sample, in order to construct the bootstrapped probability distribution, against which the empirical sample is compared. The boots trap is especially useful in cases where the probability distribution is unknown, or if the data violate certain (particularly parametric) distri­ butional assumptions . A large number of palaeonto­ logical cases fall into these categories . The boots trap method has been applied i n palae­ ontology to problems that include estimating confi­ dence limits around phylogenies, assessing patterns

495

of extinction probability and the shape of clade diversity histories, and the significance of differ­ ences in rates of evolution . A problematic feature of much palaeontological data for such methods is that the data are often ordered by (geological) time . The original bootstrap method was designed for data that are identical and independently distributed; time series do not satisfy this criterion. A method applicable to palaeontological (time series) data sampled at intervals that may or may not be constant is now available . In particular, the method recog­ nizes the necessity of coupling the magnitude of evolutionary change with the magnitude of the time interval over which that change is measured (Kitchell et al. 1987) (Section 2 . 1 1 ) . The method also works with two types of time series: those in which a change in the time series is recognized on the basis of independent criteria, and those in which a segment of the time series is identified as excep­ tional simply on the basis of that change (post hoc recognition) . Such computer-intensive methods of statistical inference will undoubtedly play an in­ creasing role in fields such as palaeontology that rely little on laws, axioms, and deductions to gain understanding. Sensitivity of initial conditions

Palaeontologists have used computer simulation methods to generate samplers of patterns produced by a variety of random processes, because much of the evidence in palaeontology since the nineteen­ seventies is pattern data. Mathematicians and statis­ ticians had already shown that random processes are capable of producing orderly pattern . Many of the properties of random processes were known by analytical solution. However, the ability to display these randomly-produced patterns graphically and by simulation did most to convince palaeontologists of the fallacy of the expectation that orderly patterns required deterministic explanations . It was shown that palaeontologically significant patterns, such as some trends and the topology of branching patterns, could be produced by random models (see review by Raup 1977) . The purpose of this work was both to enlarge the intuitive understanding of palaeonto­ logists so that they would not incorrectly equate pattern with non-randomness, and to better identify non-randomly produced patterns . The opposite side of this coin, namely that com­ pletely deterministic processes lacking randomness can nevertheless produce random patterns, required the computer for its development . Until recently

6 Infrastructure of Palaeobiology

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within all the sciences, complex patterns were con­ sidered to be the consequence of complex causes . It has now been shown, however, that apparently random behaviour can derive from even simple deterministic processes. A small difference in initial conditions, for example, can lead to unexpectedly divergent behaviours . The term 'chaos' has been applied to such patterns and processes, to dis­ tinguish them from randomness. In chaos, the dis­ order is ordered . Such ordering is apparent in the detail of the patterns, a detail made increasingly evident by computer techniques and images . In palaeontology, it was shown that the most simple model of diversification, and the one being applied to empirical analyses of taxonomic diversity,

had chaotic behaviour . Using computer simulation runs to map the surprising array of behaviours and their abrupt and ordered thresholds, Carr & Kitchell (1980) showed that the 'coupled logistic' model of Sepkoski (1979) could produce not only logistic patterns of diversity change with time but also extremely complex and chaotic patterns of diversity change . In this latter case, the oscillations are driven internally, without external perturbation. Whereas earlier work, by warning that a high degree of order can be generated by purely random pro­ cesses, had tried to dispel the palaeontologist's bias that randomness implies a random pattern, Kitchell & Carr (1985) warned against the bias that deter­ minism implies an ordered pattern . They showed

6 . 1 Computer Applications in Palaeontology that even a completely deterministic and remarkably simple process can produce patterns of bewildering complexity. The understanding of chaotic behav­ iours is now being pursued in a number of cognate fields within biology, physics, and chemistry, promising to revolutionize our collective under­ standing of a class of complex phenomena, until recently unknown .

Phylogenetic inference The methodology of inferring phylogenetic (evol­ utionary) relationships among organisms has become both increasingly explicit and empirical (Section 5 . 2) . Phylogenies are constructed from data on the distribution of characters (the empirical component, such as that resulting from morpho­ metric studies), according to some criterion made operational by a computing algorithm (the explicit component) . These criteria and associated algo­ rithms used to form phylogenetic hypotheses rely either on parsimony methods, maximum likelihood methods, or compatability methods; reviews that examine the fundamental assumptions of each method were given by Felsenstein (1983) . These methods are derived from a class of prob­ lems in mathematics and statistics that focus on maximizing or minimizing some aspect of the data. In such optimality methods, the assertion is not that the historical process of evolution is optimal. Rather, optimization methods are used to choose among all tree topologies generated by an algorithm for a given set of data. Parsimony methods, for example, evaluate phylogenetic hypotheses on the basis of number of homoplasies (convergences and parallel­ isms); the 'best' genealogy is the one of minimum homoplasy. Because the criteria for evaluating phy­ logenies are unique to the method, comparing methods in terms of finding the 'true' genealogy is not possible . Instead, types of parsimony, maximum likelihood, and compatability algorithms can be compared with one another in terms of a practical goal (efficiency in computer time) and a method­ ological goal (minimizing tree 'length' or the required independent origins of each character) . Although small data sets may be analysed by hand (using the 'brute force' method of generating all possible cladograms; there are 15 possible for four taxa), large data sets require computer-assisted analyses (there are more than two million clado­ grams for only nine taxa, and more than 1020 clado­ grams for 20 taxa) . Even the latter is too much for computer analysis . This raises an interesting situ-

497

ation; there is no exact solution to the problem of finding the minimum tree for even moderate-sized data sets . This problem may not be soluble : among mathematicians, there is agreement that NP- (not polynomial)-complete optimization problems (such as these) cannot be solved given current approaches and algorithms . Within palaeontology, phylogenetic approaches principally make use of morphological character data. An interesting discussion was pro­ vided by Gauthier et al. (1988) who showed, using both palaeontological and neontological character data, the importance of palaeontological data. Strato­ cladistic methodology may also prove useful as a means of integrating both character data and strati­ graphic data in an analysis of phylogeny, where a total parsimony debt (summed from morphology and stratigraphy) serves as the minimization criterion. A problem in need of redressing is that most palaeontological analyses of taxonomic data sets (e . g . patterns of diversity change, extinction, rates of evolution) have made use of data currently avail­ able . Much of these data do not reflect the meth­ odology discussed above . As a recognized con­ sequence, monophyletic and non-monophyletic groups are not distinguished from one another. This presents a problem of interpretation since 'monophyletic groups have a unique history that exists and is to be discovered, whereas paraphyletic groups may start off with a unique history, but their boundaries are adjusted a posteriori and they are in part a human invention' (Benton 1988) .

Computer-aided vision systems The most severe restriction on palaeontology today is the lack of adequate databases to test hypotheses of interest. It is likely that major advances in the future will be made in the rapid acquisition of morphological and character-state data from auto­ matic vision systems . Although the systems described below have not yet been widely used in palaeontology and are still in stages of development, the future of advanced computer techniques in palaeontology will undoubtedly move in these directions . With laser disc technology, it is now possible (and currently in use in some research laboratories) to store all known species' images (e . g . holotypes) and their descriptions, and to make use of them with a dichotomously driven, interactive algorithm to resolve the identification of an unknown species. This technology permits exact comparisons on the

498

6 Infrastructure of Palaeobiology

screen. Access is also virtually instantaneous, with more than 50 000 analog images currently capable of being stored per disc and with the ability to access more than one disc at a time . The system utilizes answers provided by the user to a computer-driven key to select the most likely known species . It then automatically compares the unknown image with these selected known species, making comparative diagnostic measurements. Because of the interactive nature of the algorithm, the user maintains control of the final decision. Programs designed for palaeontological appli­ cations that make use of artificial intelligence pro­ gramming have also begun to be developed (e . g . Riedel in press) . These programs explicitly attempt to deal with objects that are naturally variable (organ­ isms), and may be made even more variable by preservational processes, yet are members of a single category (the species) . These systems use character­ state descriptions entered by the user and work within a hierarchy of character-states necessary for discrimination between possible species . As above, the final result is a 'narrow as possible' reporting of species that have these characters . Algorithms associated with image analysis sys­ tems are also now available (and being developed) for converting data from serial sections of any fossil (whether actually sectioned or not) to three­ dimensional models of that fossil, thereby allowing the user in many instances to bypass the building of physical models . The reconstructed three­ dimensional form can also be viewed from all per­ spectives by rotation and movement simulation algorithms .

Acquiring morphometric data by image analysis Palaeontologists, of necessity, rely on morphological data to make evolutionary inference . A recurring problem in the sciences is that the theories of a field may occasionally far exceed the capacity of that field to acquire and analyse data necessary for evaluating those theories . Such a situation occurred in palaeon­ tology, e . g . with the proposal of punctuated equilib­ rium and its associated prediction of morphological stasis . The imperative quantitative data on morpho­ logical change within and between species, and over time and geography, were not copiously avail­ able . Much of the problem stemmed from the diffi­ culties of acqumng quantitative data on morphology in a rapid and accurate manner. Widespread interest within numerous fields in the study of biological shape and its transformation

has resulted in a series of important advances . In terms of technique, advances in computer tech­ nology have made possible increasingly powerful image analysis systems that combine image acqui­ sition and image processing capabilities with pattern recognition analyses. Such image analysis or optical pattern recognition systems have made the acquisition of quantitative data on morphology rapid, accurate, and affordable . The field o f morphometries has been redefined recently as 'the analysis of biological homology as well as geometric change' (Bookstein et al. 1985) . Morphometrics is relevant to questions of phylogen­ etics, ontogenetic trajectories and their evolutionary potential for heterochrony, patterns of anagenesis and cladogenesis, ecophenotypy, and morphologi­ cal integration. Such analyses are particularly informative when they combine hypotheses of phylogenetic descent with hypotheses of morpho­ logical (character) transformation. Reviews of methodology and examples of the application of outline methods and landmark methods were given by Lohmann (1983) and Reyment (1985), respectively. The approach rec­ ommended by Bookstein et al. (1985) focuses more on the dynamics of change in shape . Analyses begin with a study of the major dimensions of morpho­ logical variation in time and space that characterize each species . Analytical procedures determine which parameters contribute most to intraspecific characterization and to interspecific discrimination within respective geographical and temporal con­ texts. A recent application of outline and landmark methods was given by Stanley & Yang (1987) who assessed the rates of morphological evolution in separate lineages of Neogene bivalves . Schweitzer et al . (1986) used the same basic techniques to evaluate the relative contribution of development (heterochrony) and structural regulation in two closely related species .

Prospects Palaeontology today is actively engaged in computer­ aided research programs . The evolution of the interaction between palaeontology and computer technology is following much the same path as that of the evolution of the human brain, as we currently understand it. The computer has not simply resulted in an increase in the speed, efficiency, and size of the problems we analyse . It has introduced novelty or true innovation. It is well recognized that the biological and evolutionary sciences deal with a much £reater de£ree of comnlexi tv in th eir svstpms

6 . 2 Practical Techniques of study than do the physical sciences. Computer techniques are beginning to open up the field of study of complex systems and, through vision sys­ tems, to relieve the human investigator of some of the effort in amassing empirical data .

References Benton, M.J. 1988 . Mass extinction in the fossil record of reptiles: paraphyly, patchiness and periodicity (?) . In: G.P. Larwood (ed . ) Extinction and survival in the fossil record, pp . 269 -294. Systematics Association Special Volume, No. 34. Bookstein, F . , Chernoff, B . , Elder, R . , Humphries, J . , Smith, G. & Strauss, R. 1985 . Morphometries in evolutionary biology. The Academy of Natural Sciences of Philadelphia, Philadelphia. Carr, T.R. & Kitchen, J.A. 1980. Dynamics of taxonomic diversity. Paleobiology 6, 427-443 . DeAngelis, D . L . , Kitchen, J.A. & Post, W.M. 1985 . The influence of naticid predation on evolutionary strategies of bivalve prey: conclusions from a model. American Naturalist 126, 817-842 . Efron, B. & Gong, G. 1983 . A leisurely look at the bootstrap, the jackknife, and cross-validation. American Statistician 37, 36-48. Felsenstein, J. 1983 . Parsimony in systematics: biological and statistical issues . Annual Review of Ecology and Systematics 14 , 313-333. Gauthier, J., Kluge, A . & Rowe, T. 1988 . Amniote phylogeny and the importance of fossils. Cladistics 4, 105 - 209 . Gleick, J. 1987. Chaos: making a new science. Viking Penguin,

499

New York. Judson, S. 1980. The search for solutions . Holt, Rinehart & Winston, New York. Kitchen, J.A. & Carr, T.R. 1985 . Nonequilibrium model of diversification : faunal turnover dynamics. In : J.W. Valentine (ed . ) Phanerozoic diversity patterns: profiles in macroevolution, pp . 277- 309 . Princeton University Press, Princeton. Kitchen, rA. & MacLeod, N . 1988 . Macroevolutionary inter­ pretations of symmetry and synchroneity in the fossil record. Science 240, 1 190- 1993 . Kitchen, J . A . , Estabrook, G. & MacLeod, N. 1987. Testing for equality of rates of evolution . Paleobiology 13, 272-285. Lohmann, G.P. 1983. Eigenshape analysis of microfossils : a general morphometric procedure for describing changes in shape . Mathematical Geology 1 5 , 659 - 672. Raup, D.M. 1977. Stochastic models in evolutionary paleon­ tology . In: A. Hanam (ed. ) Patterns of evolution, pp. 59 - 78 . Elsevier, New York. Reyment, R.A. 1985 . Multivariate morphometrics and ana­ lysis of shape . Mathematical Geology 17, 591 - 609 . Riedel, W.R. 1989. Identify: a Prolog program to help identify variable things. Computers and Geosciences (in press) . Schweitzer, P . N . , Kaesler, R.L. & Lohmann, G.P. 1986 . Onto­ geny and heterochrony in the ostracode Cavellina Coryen from Lower Permian rocks in Kansas. Paleobiology 12, 290-301 . Sepkoski, J.J., Jr. 1979 . A kinetic model of Phanerozoic taxo­ nomic diversity. 11. Early Phanerozoic families and mul­ tiple equilibria . Paleobiology 5, 222 - 251 . Stanley, S.M. & Yang, X. 1987. Approximate evolutionary stasis for bivalve morphology over millions of years : a multivariate, multilineage study . Paleobiology 13, 1 13 - 139.

6 . 2 Practical Techniques 6 . 2 . 1 Preparation of Macrofossils P . J . W H Y B R O W & w. L I N D S A Y

Mechanical methods A rock is invariably physically weakened by the presence of fossils, usually because the chemical constituents of fossils differ from those of the en­ closing matrix. For at least three centuries, palaeon­ tologists have exploited this difference by using percussion methods, normally a hammer and a chisel, to expose and to collect fossil material. Fol­ lowing the introduction of electricity into museums and universities in the nineteenth century, power tools were developed that 'automated' the basic

manual techniques . Today, three mechanical tech­ niques are widely used in palaeontology labora­ tories: percussive, grinding, and abrasive (Rixon 1976) .

Percussive and grinding techniques. Percussive electric or pneumatic engraving pens (Fig. 1) are hand-held and equipped with a tungsten carbide tip . Invari­ ably the tip supplied by the manufacturer is too coarse for most preparations and has to be substi­ tuted by tungsten carbide rod welded onto the oscillating shank of the pen . The fitting of the rod also enables a choice of either chisel or pointed tips to be fashioned . Before commencing preparation not only should the concealed morphology of the fossil be imagined (by reference to published in­ formation concerning similar fossils) but also the petrology of the matrix must be investigated (in case acid techniques can be better utilized) . If

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6 Infrastructure of Palaeobiology state in a vibrating pressure vessel, through a nozzle of small diameter. Various hardnesses of powder can be used, ranging from sodium bicarbonate to the cast iron shot used in large industrial machines . Similarly, various diameters of nozzle can be selec­ ted . The abrasive action depends on particle size and the amount of gas pressure used . Exposed parts of a fossil can be protected by a coating of rubber latex from any polishing effect of the powder, and a box with a dust extraction system protects the oper­ ator from possibly hazardous particulates . A binocu­ lar microscope is essential for this work to see the degree or variability of abrasion of the rock.

Fig. 1 A hand-held, pneumatic engraving pen used to remove rock matrix. In the foreground is a heavy duty pneumatic chiseL

the rock cover is excessive, it can be removed by grinding . Diamond or carborundum wheels and burrs used in dentistry are ideal; for larger blocks, parallel grooves are cut using a pneumatic diamond saw and the thin rock wedges then removed by percussive methods . All preparations should be carried out at high magnifications using a binocular microscope so that the fossil -rock interface can be easily seen; a cold-light, fibre optic light source is invaluable for this (especially a system with contrasting colour filters) . The position of the per­ cussion point should ideally be at right angles to the plane of the fossil surface being exposed . The degree of force required to chip or flake away the rock and leave an unmarked specimen comes about by trial and (infrequently) error. Extreme care must be taken when microbedding planes pass through and around a fossil as flakes may contain part of it. Extensive preparation gradually weakens the structural integrity of a fossil but the percussive force used normally remains constant. Therefore, the specimen must be supported firstly by a shock absorbing cushion (such as a sandbag) and secondly by embedding in a water soluble polyethylene glycol wax of high molecular weight. For supporting delicate areas of a vertebrate skull, this wax is essen­ tial and can itself be strengthened while in its fluid state by the addition of surgical gauze (Whybrow 1982) .

Abrasive techniques. 'Airbrasive' or 'sand-blast' machines are quick and effective aids for removing rock that is softer than the fossil . An inert gas (compressed air, nitrogen, or carbon dioxide) propels an abrasive powder, which is kept in a fluid

Chemical methods

Rocks and the fossils they enclose do not always respond well to mechanical techniques . The hard­ ness of an ironstone or some limestone matrices may prohibit mechanical preparation, while the complexity or abundance of fossil remains may defy methods reliant on manual dexterity . As with mechanical methods, chemical methods aim to remove the matrix without damaging the specimen. However, in both cases, there are occasions when the information required can only be obtained by destroying the fossil and retaining the natural impression left in the rock. Chemicals used in fossil preparation are chosen for their ability to disrupt or dissolve the rock matrix, but they must achieve this without causing the same effect on the fossil. Such differentiation is determined by the chemistry of both rock and fossil. Furthermore, the long-term conservation of the fossil in a collection, with all the hazards associated with handling, must be considered .

Chemical disruption . Water, sometimes in conjunc­ tion with a detergent, readily breaks down some soft shales and muds . The clay minerals swell as the strongly polar water impregnates their structure . Detergents and other surfactants assist the process by reducing surface tension at the clay-water inter­ face . A similarly disruptive effect occurs in the presence of hydrogen peroxide (H202) . Solutions of H2 02 are unstable and deteriorate giving off oxygen . In the presence of alkalis, rough surfaces, and metals, the process is accelerated . In rock matrices the oxygen bubbles released within the pores disrupt the sediment and weaken the matrix (see also Section 6.2.2).

Sequestrants and chelating agents. Polyphosphates, such as sodium hexametaphosphate (NaP03)6, act

501

6 . 2 Practical Techniques as water softeners, sequestering the calcium, mag­ nesium, and iron salts present. Clayey and muddy sediments are broken down in solutions of poly­ phosphates. In a manner similar to that of water softeners, ch elating agents form stable complexes of metalic ions (such as calcium and magnesium) in rock forming minerals . Ethylene diaminetetracetic acid and its sodium salts in solution can corrode rock matrices, but it will also attack fossil material and careful control is therefore required .

Acids. Acids are extensively used in chemical methods of preparation (Lindsay in Crowther & Collins 1987) . Hydrochloric acid was used in the late nineteenth century to dissolve limestone con­ taining carbonized graptolites. Subsequently hydro­ fluoric, nitric, formic, acetic, and thioglycollic acids have been used in both vertebrate and invertebrate palaeontology. Hydrofluoric and nitric acids are employed for the maceration of sediment samples containing fossil pollen (Section 6 . 2 . 2) and pose particular problems of safety. The development of vertebrate material using aqueous solutions of acetic acid was first carried out in the nineteen-forties and followed from earlier techniques devised at the British Museum (Natural History) (Rixon 1976) . Acetic acid is the most commonly used acid for this work and is readily controlled and reasonably safe at low concen­ trations . Used in solutions of 1 - 10%, the reaction between the acid and calcium carbonate in the matrix occurs more readily than that between the acid and phosphates in fossilized bone (Fig. 2) . The differential rate of dissolution is controlled by vary­ ing the length of immersion time and the acid concentration . The time of exposure to acid at each step of the process may vary from a few hours to several days, and the development of a specimen may take years to complete . Bone that undergoes prolonged exposure to acid will be significantly affected; for this reason the dissolution of the matrix is interrupted regularly to wash, dry, and lacquer any newly exposed bone .

Consolidants and adhesives Consolidation (hardening) of a specimen must be carried out during preparation in order to conserve it for subsequent study. A number of adhesives and consolidants are used; they should be reversible in the long term as further work on a specimen may be required . In mechanical preparation the surface of the fossil is coated with a consolidant as the rock is removed in order to prevent fractures caused by

Fig. 2 The partially exposed, post cranial skeleton of the Jurassic dinosaur Scelidosaurus harrisoni during preparation with acetic acid.

I I I I I I

Anterior skull and jaw elements of the Lower Cretaceous dinosaur Baryonyx walkeri after mechanical and chemical preparation. Scale in cm . Fig. 3

any excessive vibration (Fig. 3) . Polyvinyl butyral resin, dissolved in a variety of solvents, has now replaced polyvinyl acetyl resins and serves as an adhesive when dissolved in ethyl acetate . Poly­ methyl-methacrylate, also dissolved in ethyl acetate, is a useful adhesive but shrinks markedly on drying and should never be used as a consolidant. Supplied as a powder monomer with a liquid polymer cata­ lyst, polymethyl-methacrylate effectively seals wide cracks . Cynoacrylate adhesives are effective for the fast repair of small pieces of fossil, but their long­ term stability is at present poorly understood and they are practically insoluble when set. Chemical methods of preparation require adhesives and consolidants that protect the fossil from chemical attack as well as supporting and strengthening it.

6 Infrastructure of Palaeobiology

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Polybutyl-methacrylate is used as an acid resistant con solid ant and can withstand long periods of immersion in acids . Polymethyl-methacrylate as an adhesive is similarly resistant to attack by organic acids; the cynoacrylates also seem to be unaffected. In all methods of preparation, which by necessity expose the fossil to risk, good records must be kept (Rixon 1976) . Photographs, drawings, and written descriptions are essential and must be prepared as the specimen passes through various stages of treat­ ment. Their value can only be appreciated when a dismembered fossil needs to be reassembled .

References Crowther, P.R. & Collins, C]. (eds) 1987. The conservation of geological material. Geological Curator 4, 375 -474. Rixon, A . E . 1976. Fossil animal remains: their preparation and conservation . The Athlone Press, London . Whybrow, P.J. 1982 . Preparation of the cranium of the holo­ type of Archaeopteryx lithographica from the collections of the British Museum (Natural History) . Neues Jahrbuch fUr Mineralogie, Geologie und Paliiontologie Mh H3, 184- 192.

6 . 2 . 2 Extraction of Microfossils R . J . A L D RI D G E

Extraction techniques have been developed princi­ pally to recover microscopic fossils from rock samples, but may also be adopted for larger speci­ mens . A variety of chemical and mechanical pro­ cedures for rock disaggregation are employed, dependent upon the composition of the rock and of the fossils sought. Residues from these processes are often large, and some concentration of the micro­ fossil specimens may be required . Many of the chemicals used in dissolving samples and in concen­ trating residues are highly hazardous or toxic and the safety aspects of all techniques should be fully investigated before they are applied . Full attention must be given to hazard warnings given by the suppliers of chemicals .

Releasing microfossils from rocks

Calcareous rocks. Limestones, dolomites, and cal­ careous clastic rocks can be broken down with dilute organic acids (e .g. acetic acid, CH3COOH;

formic acid, (HCOOH) to release microfossils com­ posed of calcium phosphate (conodont elements, fish remains) or with resistant organic walls (sco­ lecodonts, chitinozoans, palynomorphs) (Fig. 1 ) . Some workers crush the samples into 1 - 3 cm chips, but this is only necessary for very impure lime­ stones . Standard procedure is to place the sample in a polythene bucket or beaker which is then filled with warm, 10- 15% acetic acid; formic acid acts more rapidly and may be used at higher concentra­ tions, but is more corrosive and hazardous . Phos­ phatic material may be attacked by acetic acid in the absence of calcium acetate to buffer the sol­ ution, so powdered calcium carbonate should be added to samples with low lime content. Alter­ natively, samples may be buffered by using a sol­ ution comprising 7% concentrated acetic acid, 63% water, and 30% of filtered liquid remaining after digestion of previous samples . Hydrochloric acid (HCl) dissolves phosphate, but may be used at a concentration of about 10% to recover organic-walled microfossils and siliceous (e . g . radiolarians) or silicified material. When buf­ fered by calcium acetate, HCl can be used to extract phosphatic, siliceous, and organic specimens from a single sample, but there is always a risk of damage to the phosphate, especially when all the limestone is allowed to dissolve . When effervescence fades or ceases, the sample is sieved; the mesh sizes of the sieves employed are dictated by the sizes of the microfossils sought. For conodont elements, an upper sieve of 1 mm mesh and a lower of 75 [tm are adequate, but chitinozoans and palynomorphs require much finer bottom sieves, down to 5 [tm. Undissolved rock remaining on the upper sieve is placed in new acid solution, while the sieved residue is dried and retained for concentration and picking. There is no easy technique for recovering cal­ careous microfossils from calcareous rocks . Soft limestones and marls may be treated in a similar way to soft shales, but for hard limestones and chalks only crude mechanical methods are available . Normally, these involve pounding the moistened sample with a pestle in a mortar, followed by wash­ ing and concentration . An intermediate step is sometimes inserted in which the pulverized sample is washed into a container and placed in an ultra­ sonic cleaner for a period of two minutes to two hours . Delicate microfossils will not survive these techniques and are best studied in thin section. The procedure may be successful, though, for calcareous nannofossils such as coccoliths .

6 . 2 Practical Techniques

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Fig. 1 Techniques for extracting and concentrating microfossils from limestones, calcareous clastic rocks, and soft or partly indurated mudrocks .

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Argillaceous rocks. Soft or partly indurated clays and shales may be disaggregated by a number of tech­ niques . A relatively gentle procedure involves the use of petroleum ether, paraffin, or similar solvent on thoroughly pre-dried samples (Fig. 1 ) . All of these solvents are highly flammable, and due regard must be given to fire risks . The rock is soaked in solvent for at least one hour; the solvent is then poured off and the rock immediately inundated with hot (not boiling) water. The clay is reduced to an uncohesive, muddy slurry, which then can be wet-sieved as appropriate . Black shales and other mudrocks that do not respond to this treatment may disaggregate on immersion in a 10- 15% solution of hydrogen peroxide (H202) in water (see also Section 6 . 2 . 1 ) . The reaction involves the oxidation of organic matter, which may also be accomplished by other oxidizing agents, such as sodium hypochlorite (NaClO) . Hard clays may also disintegrate when boiled in water with a dispersing agent. Those commonly used include a few grams of sodium carbonate (Na2C03) or 20% sodium hydroxide (NaOH) . Some

samples respond to boiling in the detergent Quat­ ernary '0', with a 20% solution added to boiling water containing the sample . A combination of techniques may be applied, perhaps involving treat­ ment with buffered acetic or formic acids for samples containing some calcium carbonate . Mechanical disaggregation may sometimes be achieved by alter­ nate freezing and thawing of samples soaked in water, or by boiling the rock in sodium thiosulphate (Na2S203.5H20), which will crack the shale apart as it crystallizes when allowed to dry.

Sandstones. For most microfossils there is no tech­ nique for extraction from sandstones or siltstones, unless the rock is poorly-cemented, when mechan­ ical methods may be successful, or calcareous, when acids may be employed . For organic-walled micro­ fossils, palynological techniques (below) may be tried, but palynomorphs are not normally well preserved in coarse clastic rocks . Cherts. Phosphatic microfossils, such as conodont elements, can be recovered from cherts and other

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6 Infrastructure of Palaeobiology

siliceous rocks using dilute hydrofluoric acid (HF) . The sample is crushed into 1 - 5 cm fragments, any carbonate removed with acetic acid, and the frag­ ments placed in 5 - 10% HF in an acid-resistant plastic container in a fume cupboard . After 24 hours the HF is decanted off and neutralized with calcium hydroxide; the residue is first washed with dilute HCl, then several times with water before being sieved and reprocessed as necessary . The technique works through fluoridization of the apatite of the conodont elements and is accompanied by some fracturing and distortion of specimens . Hydrofluoric acid is extremely dangerous and must be used in properly designed fume cupboards with the handler wearing full protective clothing.

Concentration techniques Residues from disaggregation procedures can be concentrated into light and heavy fractions by using various heavy liquids . Bromoform (CHBr3, specific gravity 2 . 89) and tetrabromoethane (C2H2Br4, specific gravity 2 . 96) are commonly used to produce a heavy concentrate containing phosphatic micro­ fossils, but these chemicals are severely toxic. A safer alternative involves the use of water-soluble sodium polytungstate (3Na2W04.9W03. H20), which can be made up at any required specific gravity, but is best at 2 . 75 or slightly higher to avoid problems of high viscosity and crystal precipitation . Light or buoyant microfossils, such as hollow foraminiferans, radiolarians, and chitinozoans, may be removed in a light concentrate by adjusting the specific gravity of the sodium polytungstate accord­ ingly. Electromagnetic separation is useful in deal­ ing with large residues containing iron oxides or iron-rich dolomite grains .

(nitric acid) prior to crushing to 1 -2 mm fragments . Any carbonate in the rock must be completely re­ moved using warm 10% HCl, followed by thorough washing in distilled water. Silica and silicates are dissolved using HF . Cold, concentrated HF is poured onto the sample in a polypropylene beaker and stirred daily with a teflon rod until all the rock has disaggregated . The reaction may be speeded up by warming the containers in a water bath . After digestion the sample is washed with warm water and fluoride precipitates are removed by treatment with warm 40 -50% HCl, followed by at least four washes in warm water. Ten per cent HCl is added to the last washing to discourage flocculation . Mineral particles may be separated from the organic residue by centrifuging in zinc bromide solution (specific gravity 2 . 0); if examination reveals the presence of pyrite, 10% HN03 may be added to the organic fraction for ten minutes to remove it. Unwanted, undecomposed, or partially decomposed organic material can be removed by careful oxidation (although experience is needed to avoid destruction of microfossils during this process) . Concentrated HN03 is a commonly used oxidant. Fine organic debris may be removed by alkali treatment with 5% potassium hydroxide (KOH) . After processing, the remaining organic-rich resi­ due is sieved, using appropriate mesh sizes for the palynomorphs present. Generally a 53 !-tm sieve is employed to retain chitinozoans and large paly­ nomorphs, while a fine sieve of 5 - 7 !-tm is necessary for the smallest specimens . The fossils may be further concentrated prior to sieving by swirling in a large watch glass . The palynological concentrate, or a representative fraction of it, is finally strew­ mounted onto slides, using glycerine jelly for tem­ porary mounts and Canada balsam or a plastic mounting medium for permanent mounts .

Palynological techniques Procedures for the recovery and concentration of palynological microfossils are complex, with the steps tailored to the nature of the sample being processed . A full account was given by Phipps & Playford (1984), who emphasized the dangers of HF, zinc bromide (ZnBr2), and other chemicals used.

Palynological processing should only be undertaken in a purpose-built laboratory with efficient fume-cup­ boards, full protective clothing, and neutralization and disposal facilities available. All equipment must be kept absolutely clean to avoid contamination . Rock samples should be thoroughly cleaned by scrubbing and, if necessary, etching in HCl or HN03

References Austin, R.L. (ed . ) 1987. Conodonts: investigative techniques and applications . Ellis Horwood, Chichester. Brasier, M.D. 1980 . Microfossils . George Allen & Unwin, London. Phipps, D . & Playford, G . 1984. Laboratory techniques for extraction of palynomorphs from sediments . Papers, Department of Geology, University of Queensland 11, 1 -23 .

6 . 2 Practical Techniques

6 . 2 . 3 Photography D . J . SIVETER

Introduction The photography of fossils involves a wide range of techniques, materials, and object sizes . Large fossils, in excess of about 15 cm in length, fall within the range of normal cameras with standard lenses; specimens up to about 2-3 mm long are best photo­ graphed using the scanning electron microscope (SEM). The middle ground between normal and SEM photography (Section 6.2.4) is generally known as macrophotography, and covers a magnification range on the negative from about x 0 . 2 to x 20 or more . Macrophotography in incident light, for which there are numerous systems available, is the type of photography used for most macroinvertebrates . The Leitz 'Aristophot' system (Whittington in Kummel & Raup 1965) was first used for the macropho­ tography of fossils in the nineteen-fifties, and has since been widely adopted (Fig. IH) . It was modified in various ways before production was discontinued in the early nineteen-eighties . In its image range the quality of photographs produced by this appar­ atus is excellent . The comparable Nikon 'Multi­ phot' system gives similar results and is still (1991) marketed. In the last decade Wild-Leitz (now Leica) have introduced a quite different system for the macrophotographic range, the photomacroscop . The most useful source on the photography of fossils is Kummel & Raup (1965); many of the techniques described therein have not been superseded.

Preparation: cleaning and coating Prior to photography any extraneous sediment should be removed from the surface of the fossil (Section 6 . 2 . 1 ) . If the specimen is embedded in matrix, particular effort should be concentrated on cleaning its margins . This obviates the need for any retouching of or cutting round the fossil outline to delete non-organic material on the final print. The handling of testaceous specimens should be mini­ mized, and they should be cleaned with an organic solvent (such as acetone) to remove any surface grease marks . When photographing most fossils, particularly those that are of variable or light shade, better

505

results are obtained if the specimen is first coated. A matt, uniformly dark surface is applied to the fossil which is then lightly dusted with a whitening agent for contrast. Fountain pen ink and particularly black photographic opaque have been used as darkening agents; these should ideally be applied to impart a dark grey (not black) colour. The former can be removed in large part with a mixture of ammonia and hydrogen peroxide solutions, and the latter with warm soapy water. The cleaning of darkening agents from natural mould specimens (especially in medium to coarse clastics) is very difficult or impossible, as they are fully absorbed into porous sediments; this is particularly so where Indian ink has been used . The excellent opaque produced by Phillips and Jacobs (Philadelphia) is now discontinued . Practitioners should experiment with alternatives; poster paint has, for example, been successfully used . Various inks and carbon powder (soot) have been used to darken latex and silicone rubbers . A whitening agent sympathetically applied on the darkened surface considerably enhances the contours and surface sculpture of the fossil, as it falls more densely on those areas of greater relief, which are thus highlighted (Fig. 1 ) . It also provides an even, glare-free reflecting surface for photogra­ phy and results in prints of a similar tone - which are desirable when making plates for publication. Ammonium chloride, magnesium oxide, and anti­ mony oxide have all been used for whitening. Ammonium chloride and antimony oxide are heated in a glass bulb and the resulting sublimate cloud directed onto the fossil (Teichert 1948; Marsh & Marsh 1975) . Magnesium oxide is produced by burning magnesium ribbon and the fossil is held over the smoke . Ammonium chloride should be washed off immediately after use as it combines with water vapour in the air to form hydrochloric acid capable of etching the fossil; its deliquescence also renders it impracticable for use in areas or on days of high humidity, as the sublimate quickly becomes coarse-grained after coating. Nonetheless, many authors favour the use of ammonium chloride as control on the application of magnesium oxide is not very precise . All coating should be done in a fume cupboard, but the draught should not be so strong as to affect the flow direction of the whitening agent. After coating and prior to photography a check should be made under a binocular microscope for hairs or other artifacts . The implications for future conservation of the specimen should be considered before employing these techniques .

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Fig. 1 A and B taken using Nikon 'Multiphot', C -G using Leitz 'Aristophot' . A taken with the Nikon 'Makro-Nikkor' 12 cm lens, B with Nikon 'Makro-Nikkor' 6.5 cm lens, C - G with the Leitz 'Summar' 12 cm lens . A - C, E, G photographed on Kodak 'Panatomic X' film, D and F on Ilford 'Pan-F film. All specimens are coated with ammonium chloride on top of matt black opaque. A-G, Silurian trilobites . A, Cranidium, odontopleurid, Ireland; dorsal view, x 4. B, Glabellar sculpture, proetid, Ireland; dorsal view, x 22 . C, Thoracic pleural facet, calymenid, Gotland; lateral view, x 10. D, Stereo-pair, complete specimen, calymenid, West Midlands, U.K. ; dorsal view, x 2. E, Glabellar sculpture, calymenid, Welsh Borderland; dorsal view, x 10. F, Eye, phacopid, Ireland; oblique view, x 7. G, Complete specimen, calymenid, Gotland; oblique view x 2.5. H, Leitz 'Aristophot' with anglepoise and ring light illumination, laboratory jack, and tilt-table for taking stereo-pairs.

6 . 2 Practical Techniques Macrophotographic equipment and methods The photographic film should be fine grained (50 ASA or less) and have good resolving properties so that when enlarged it suffers minimal loss of definition; Ilford 'Pan-F' and Kodak 'Panatomic X' are both suitable . Fossil size on the final print depends on the negative magnification multiplied by that selected on the enlarger. Macrophotography of fossils is for most purposes adequately and econ­ omically performed with the use of 35 mm format, with final prints of up to X 30 to X 40 being satisfactorily obtained . Recourse to larger format apparatus and film (e . g . 9 X 12 cm) is preferable only where excessive enlargement is demanded, or where a wider field of view is required at a given magnification . The photographic stand should be sturdy and capable of absorbing vibrations . The camera body is not one of the more critical pieces of equipment but the action of the shutter should be smooth if this is to be used to control exposure, and those with a reflex mirror lock-up facility that negates the vibrations from this source are most useful . Leica 'M' cameras have been used on the 'Aristophot' in combination with a separate reflex mirror unit that also incorporates a focusing magnifier and focusing screen . Nikon 'F' cameras for use with the 'Multiphot' house the reflex mirror and focusing system within the camera body . At high magnifications requiring long bellows exten­ sions, where the slightest vibration is ruinous, it is best to control the exposure by means of the lens shutter rather than the camera shutter . When using the 'Aristophot' in the 35 mm format, the correct exposure time is best assessed empirically with the use of test films and records of film speed, lens type, aperture setting, lighting, and magnification . Through the lens metering (TTL) is available in this format with the 'Multiphot', utilizing in particular the Nikon F3 camera . However, with over-long exposures (in excess of about 1 second the readings from any type of metering system will be inadequate due to reciprocity failure, and extra time must be allowed, depending on the film type. Much macro­ photography of fossils falls within the 1 - 15 second exposure time . The focusing screen on the camera should be of the finely ground glass or clear glass type and focus­ ing done at full aperture . The specimen - lens and lens - film (bellows length) distances combine to determine magnification on the negative, and at any given magnification these distances will vary according to the focal length of the lens employed .

507

Manufacturers' handbooks normally contain graphs plotting magnification against distance for each lens . Sometimes it is desirable to produce negatives at set, whole number magnifications; this requires retention of the camera and lens in the appropriate positions and focusing by moving the specimen vertically, either by means of a heavy duty labora­ tory jack or a rack and pinion operated 'lift' . The specimen can be mounted by plasticine onto the jack or 'lift', the surface of which should be painted matt black to provide a contrasting background to the whitened fossil . Photographs other than those of surface sculpture should not be focused on the upper surface of the fossil but more towards the median plane of the specimen to take into account depth of field . Lighting comprises two basic components . A directional light source, by convention shining from the northwest, is beamed at the fossil at an angle (normally low) suitable for emphasizing its relief. The shadows thus produced are partially filled in and the specimen lit overall by means of soft, dif­ fuse, even illumination . One of the several ways of achieving the desired effect is to use an anglepoise lamp with a frosted bulb, the light strength of which is controlled by a dimmer switch, together with a fluorescent ring light (about 30 cm diameter and 60 watts) capped by a reflector (Fig. IH) . Any extraneous light should be prevented from entering the lens . It is important to ensure that any lens used for enlarging small objects gives, in addition to sharp resolution at the plane of focus, good imaging throughout the depth of the specimen . Increased depth of field is achieved by reducing the size of the lens aperture, but beyond a certain limit (which can be empirically determined for each lens) the effect of diffraction gives progressively poorer resolution and makes it pointless to stop down further . Lenses optically corrected for the macrophotographic range, for use with the ' Aristophot' or 'Multiphot', come in several focal lengths from about 12 mm to 120 mm. Lens selection depends on the desired scale of repro­ duction, those with shorter focal lengths being used for greater magnifications . The original 'Aristophot' lenses, the Leitz 'Milar' and particularly the 'Summar' range, and also the later, compatible first generation 'Photar' range, give excellent results; Nikon have consistently produced four macro lenses with high resolving power for use with the 'Multi­ phot' . The latest, more restricted generation of 'Photar' lenses reproduce over the X 1 to X 16 range and are combined with the Leica 'R' system of

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cameras and bellows, featuring through-the-Iens metering, for use on a copying stand . Other Leica 'R' macro lenses for use with this system enable reproduction from infinity to X 3 . The 'M400' photomacroscop o f Wild-Leitz i s a fully integrated unit featuring 35 mm to 9 x 12 cm format, automatic exposure control, and a 1 : 5 macrozoom objective, focusing being accomplished via a binocular system. With the optional use of three additional objectives and using the 35 mm format it covers the macro range X 1 to X 20 . A I : 6 'Apozoom' objective has recently been introduced for this set-up . Wild-Leitz also offer a similar auto­ matic system in the macro range on their 'M420' zoom macroscop . It is debatable whether the macro­ zoom lenses used on these systems can out-perform the individually computed Leitz or Nikon macro lenses, although the photomacroscop would seem to win over the 'Aristophot' and 'Multiphot' in terms of convenience of operation, combined with the relative lack of experience required to obtain reasonable results.

Special techniques More specialist techniques are sometimes em­ ployed in the macrophotography of fossils . Stereo­ photography involves photographing the specimen in two slightly different attitudes differing by an angle of rotation of 7- 10° (Fig . 10) . The resultant two photographs give a three-dimensional image when optically fused by means of a steroscope (Evitt 1949) . Immersion of a specimen in a liquid such as alcohol, water, glycerin, or xylene is under­ taken particularly if the fossil is of low relief, and where the distinction between the fossil and the surrounding matrix needs enhancement, and also to make clearer internal structures (Rasetti in Kummel & Raup 1965) . Photographs taken in ultraviolet radiation at low inclinations also bring out features of low relief (e . g . Whittington 1985) . Lastly, X-ray photography with the use of long exposures has been successfully employed on pyrit­ ized material (StUrmer et al. 1980) . A combination of the above techniques is possible, as with stereo and X-ray photography .

Processing and printing A fine grained developer should be used for the film, to maintain detail . The enlarger should have a good quality lens and hold the film perfectly flat. Resin coated paper has advantages over tra-

ditional fibre-based paper in speed of development, fixing, and washing, and the fact that glazing is un­ necessary - it can be simply air-dried if required . Multigrade paper (either fibre-based o r resin coated) is convenient to use and enables very fine contrast control on the finished print by utilizing enlarger filters graduated to half a grade of monograde papers; it also makes redundant the potentially wasteful practice of having five boxes of different grade paper open simultaneously . Glossy paper pro­ vides a wider range of contrast and tone, and more detail than matt paper . Optimum use of space and prints of matching tone with parallel edges are necessary for an aesthetically pleasing plate (Fig . 1 ) .

References Evitt, W.R. 1949 . Stereophotography as a tool of the paleonto­ logist. Journal of Paleontology 23, 566- 570. Kummel, B. & Raup, D . 1965 . Handbook of paleontological techniques . W.H. Freeman and Co . , New York. Marsh, R . e . & Marsh, L . F . 1975 . New techniques for coating paleontological specimens prior to photography . Journal of Paleontology 49, 565 -566 . StUrmer, W., Schaarschmidt, F. & Mittmeyer, H.-G . 1980. Versteinertes Leben in Rontgenlicht. Kleine Senchenberg­ Reihe No. 11, Verlag Waldermar Kramer, Frankfurt am Main. Teichert, e. 1948 . A simple device for coating fossils with ammonium chloride. Journal of Paleontology 22, 102- 104. Whittington, H . B . 1985 . The Burgess Shale. Yale University Press, New Haven.

6 . 2 . 4 Electron Microscopy

D . CLAUGHER & P . 0 . TAYLOR

Both the transmission (TEM) and scanning (SEM) electron microscopes have wide-ranging appli­ cations in palaeobiological research, including studies of skeletal microstructure and growth, func­ tional morphology, and taphonomy .

Transmission electron microscopy The TEM produces an image by passing a beam of electrons through a specimen which must be very thin (90 - 250 nm) and must fit onto a 3 . 5 mm dia­ meter microscope grid . Methods for investigating fossils using the TEM were developed in the early days of carbon replication . This technique involved

6 . 2 Practical Techniques coating a specimen with carbon, dissolving the specimen, and examining the carbon replica of the specimen surface in the microscope . Although much useful information could be gained using carbon replicas, the technique was relatively unpopular because of limitations on specimen orientation in the microscope, and the delicate nature of the rep­ lica. Before the advent of SEM, however, small speci­ mens, such as coccoliths and diatoms, and fragments of larger specimens were routinely examined in this way. Fossil plant and animal tissue is generally miner­ alized and unsuitable for direct study with the TEM. However, unmineralized tissue may be prepared for TEM examination by releasing it from the matrix using acids or other solvents . The released tissue is thoroughly washed in distilled water to remove any remaining acids or solvents, and is then dehydrated through a graded series of acetone solutions . After two changes in pure acetone, it is embedded in an epoxy resin. Sections are cut with a glass or diamond knife on an ultramicrotome, then mounted on grids, dried, and examined in the TEM (see Glauert 1974) . Using this method Urbanek & Towe (1974) were able to produce some excellent micrographs of unstained graptolite tissue, and the palaeobotanical literature contains many similar examples .

Scanning electron microscopy The introduction of the SEM in 1968 gave palaeon­ tologists an instrument of such versatility that 20 years later new techniques for investigation are still being developed . The SEM produces an image by bombarding the surface of a specimen held in a high vacuum with a stream of electrons . This pro­ vokes the generation of X-rays, secondary electrons, and backscattered electrons, which may be collected and processed to form a visual image of the speci­ men on a cathode ray tube (see Goldstein et al. 1981 ) . The method is non-destructive, and some microscopes can accommodate specimens up to 10 cm in diameter. Stereoscopic images can be prepared with SEM . Two photographs are taken at a separation of 8° and, when examined using a stereo viewer, these may give much additional information on the spatial arrangement of the specimen. Good examples of this application can be found in issues of A Stereo-Atlas of Ostracod Shells (British Micro­ palaeontological Society, London) . A disadvantage of the early SEMs was that all

509

material to be examined had first to be coated with a thin layer of conducting metal such as gold, plati­ num, or aluminium. Many museum curators are unwilling to commit type or other valuable speci­ mens to this treatment, despite the fact that some coatings can be subsequently removed (e . g . gold by treatment with cyanide) . A device known as CFAS (charge free anticontamination system) is now available which allows uncoated specimens to be examined (Taylor 1986) . The microscope chamber is pumped to a poorer vacuum than the gun and column, and a back scattered electron detector is used in place of the normal secondary electron detector to collect the signal. Specimens do not have to be glued or permanently attached to a stub, but are simply held on a metal plate with plasticine or a similar substance which does not contaminate the inside of the microscope . Clear micrographs of un­ coated specimens can be obtained using CFAS (compare Fig . lE, F) . The coating of valuable specimens may also be avoided by preparing replicas (Fig. lC) for examin­ ation in the SEM. Hill (1986) investigated various replicating materials and concluded that cellulose acetate (which must be used with care on delicate material) gave the best results, whereas the more commonly used latex rubber gave poor results . The method of attachment specimens to stubs is of paramount importance, especially if the specimen is later to be recovered for examination of the reverse side . Double-sided adhesive tape is commonly used because it is convenient and permits specimen re­ moval using an organic solvent . However, this is not a recommended procedure; the volatile compo­ nents of the adhesive tape evaporate in the micros­ cope and deposit in the form of carbon on the inside of the column and apertures, giving rise to poor image resolution. A simple and inexpensive method for attaching microfossils (e . g . foraminifera, pollen, and spores) and small fragments of macro­ fossils is as follows: (1) cut dried processed film into small squares and glue it to stubs with the emulsion side of the film uppermost; (2) moisten a small area of the film with water using a fine paintbrush to soften the gelatin; and (3) manipulate the specimens onto this area and leave them to dry (after examin­ ation, removal or re orientation can be achieved using a wet paintbrush) . Permanent attachment of material to stubs should be made with epoxy resin (not the quick setting varieties, which may not set as hard as normal types) . Only small quantities of epoxy should be used for small specimens, and special care should

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6 Infrastructure of Palaeobiology

Fig. 1 Scanning electron micrographs illustrating some of the diverse palaeobiological applications of the SEM . A, Umbilical view of the benthic foraminifer Pseudorotalia yabei (Ishizaki), a species from the Miocene of Borneo potentially useful in stratigraphy, x 33. (Micrograph courtesy of Dr r E . p . Whittaker . ) B, Proximal end of a rodent femur from a British Pleistocene cave site showing evidence of digestion by a predator, x 10. (Micrograph courtesy of Dr P.J. Andrews. ) C, Dow Corning silicon rubber replica of in situ spores of the fern Qasimia schyfsmae (Lemoigne) from the Permian of Saudi Arabia, x 1000. (Micrograph courtesy of Dr CR. Hill) . D, fractured shell of the British Jurassic bivalve DeItoideum delta (Smith) showing prismatic microstructure with endolith borings, x 335 . E,F, part of a colony of the bryozoan Metrarabdotos moniliferum (Milne Edwards) from the Pliocene of U.K. depicted as a conventional secondary electron image of the gold-coated specimen (E) and a backscattered electron image of the uncoated specimen (F) prepared using CFAS, x 13.

511

6 . 2 Practical Techniques b e taken with porous material which tends t o absorb the adhesive and in some cases obscures surface detail . For very small fossils (e . g . diatoms), which are not practicable to mount individually, the fol­ lowing method is advocated: (1) abrade a clean stub with very fine wet and dry emery paper, wash thoroughly in an ultrasonic bath and dry; (2) rub epoxy resin into the abraded surface using a cocktail stick and remove the excess adhesive with a lint­ free tissue such as 'vellin' to leave the epoxy only in the very fine grooves; and (3) onto this surface place the specimens which will adhere permanently . Coccoliths are among the most difficult fossils to prepare, but dry material can be treated as above if the stub is very finely abraded and the excess epoxy wiped off very thoroughly. The most successful method for mounting coccoliths is simply to abrade a stub with very fine emery paper, wash, dry, and then pipette a suspension of material onto the stub; dry and coat before examining. Many fossils in the SEM accumulate charge which degrades image quality. Charging may be related to the composition of the specimen, poor attachment to the stub, or inadequate coating. The use of CFAS, a backscattered electron detector, or reduction of the accelerating voltage may eliminate charging but often does so at the cost of poorer resolution . One of the most promising developments to help overcome the charging problem is a method of collecting and pro<;essing the signal prior to recording it, known as scanstore. The last and most successful method is the use of a Field Emission SEM. This instrument produces a thousand times more electrons than a conventional SEM and can be operated at very low voltages without apparent loss of resolution . Quantitative and qualitative analysis of elements can be undertaken with suitably equipped SEMs (and also TEMs) . Analysis is usually best carried out on flat specimen surfaces, but new computer con­ trolled and corrected systems can allow analysis of rough surfaces .

References Glauert, A.M. (ed . ) 1974. Practical methods in electron micro­ scopy. Vol . 3. North Holland Publishing Co. , Amsterdam . Goldstein, J . I . , Newbury, D . E . , Echlin, P . , Joy, D . C . , Fiori, C . & Lifshin, E . 1981 . Scanning electron microscopy and X-ray microanalysis . Plenum Press, New York . Hill, C R . 1986 . The epidermis/cuticle and in situ spores and pollen in fossil plant taxonomy. In : R.A. Spicer & B.A. Thomas (eds) Systematic and taxonomic approaches in palaeobotany, pp . 123- 136 . Systematics Association Special Volume, No . 31 .

Taylor, P . D . 1986 . Scanning electron microscopy of uncoated fossils. Palaeontology 29, 685 -690 . Urbanek, A. & Towe, K.M. 1974. Ultrastructural studies on graptolites, 1 : the periderm and its derivatives in the Dendroidea and in Mastigograptus . Smithsonian Contri­ butions to Paleobiology 20, 1 - 48.

6 . 2 . 5 Determination of Thermal Maturity J . E . A . MARSHALL

Introduction Fossils, in addition to their importance in biostrati­ graphy, are invaluable as indicators of thermal maturity or rank. The fossil groups used are exclus­ ively microfossils and have to be organic (e . g . spores) o r have a n organic component i n a mineral­ ized wall (e . g . conodonts) . Such microfossils indi­ cate thermal maturity because their organic matter alters through progressive burial. As temperature increases with depth, hydrogen and oxygen are lost in excess to carbon, which changes physical proper­ ties such as colour, reflectivity, and fluorescence . Thus measurement of these properties is an estimate of the maximum temperature reached, although de­ termination of exact values is complicated by factors such as time . Not all methods are of equal value for the different microfossil groups, or applicable throughout the geological column .

Vitrinite reflectivity The origins of thermal maturation studies lie in the investigation of coal rank and particularly the optical properties of coal revealed by incident light exam­ ination of polished blocks . (If light is shone on the polished coal surface a consistent amount is reflected back, proportional to burial depth . ) The coal maceral adopted for measurement is vitrinite; the rank indi­ cator is known as vitrinite reflectivity and is ex­ pressed as a percentage . Vitrinite is not restricted to coals and is found widely dispersed in dark mud­ rocks (but not carbonates) . Measurement is made on a microscope equipped with a photometer and

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6 Infrastructure of Palaeobiology

stabilized power sources; the sample is observed using oil immersion objectives to obtain sufficient contrast to resolve individual macerals . Measure­ ments are made relative to a standard of known reflectivity for calibration. Reflectivity determi­ nation is routine, although difficulties can be encountered in identifying vitrinite and discrimin­ ating between types of vitrinite which behave differently during maturation . There is also the phenomenon of suppressed reflectivity values in amorphous organic matter (A . a . M . ) kerogen rich in as opposed to woody dominated kerogen - the former showing systematically lower values . This effect must be considered when comparing samples, or in calibration against temperature . The relationship between temperature and vitri­ nite reflectivity is not simple : time must be con­ sidered in addition to maximum temperature (time -- temperature dependence remains a contro­ versial subject, but the concensus is moving towards temperature as the single factor) . Temperature values corrected for the effect of time can be esti­ mated directly from a Karweil type diagram (Fig. 1) in which both are cross plotted against a series of reflectivity values . More complex models are also used, which involve a detailed burial history rather than a single heating event. In many instances vitrinite reflectivity is used as a thermal index with­ out recourse to temperature conversion and, as such, is the most widely accepted indicator of hydro­ carbon generation . Hydrocarbons, such as oil and gas, are generated by the action of heat on kerogen over time, so vitrinite reflectivity values may be used to define the major phases of generation . In general, reflectivity values below 0 . 5% show that no hydrocarbons have been generated, whilst the range 0 . 5 - 1 . 3% defines the oil window where the bulk of hydrocarbons are produced. Gas production continues above 1 . 3% . Spores and pollen

Colour. The colour of spores and pollen is the second most important index of organic maturity after vitrinite reflectivity . When determining colour in spores and pollen it is important always to select taxa of similar construction, as variation occurs in any assemblage . It is good practice to select simple spores and pollen with a 'single' unpigmented wall and without prominent sculpture; the sacci of bisaccate pollen satisfy these criteria and are ubiquitous in most Permian to Recent sediments .

� ;:>

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A Karweil type diagram from which maximum temperature can be determined from known vitrinite reflectivity and estimated duration of heatinglburial. (From Bostick et al. 1979 . )

Fig. l

Colours are estimated on a visual scale (Fig . 2) by reference to a set of spore/pollen standards (most of which have been produced by commercial labora­ tories and are therefore not widely available because of cost and confidentiality) . The range of colour in spores is continuous and the scale boundaries are imposed arbitrarily. The colours are also difficult to describe in words so that, without recourse to standards, these scales can only be crudely applied . They are also frequently non-linear when compared to both depth of burial and other maturity indicators; brown and darker colours become unpredictable in their occurrence, rendering the scales of limited value at higher temperatures . The influence of time is important since changes in colour are not instantaneous . Thus a time - temperature cross plot like that used for vitrinite can be employed (Fig . 3) to estimate maximum temperature . The correlation of colour against vitrinite reflectivity in different depositional basins does not give a constant relationship since these materials behave differently kinetically. Differing geological histories result in different durations of thermal input and each basin has a somewhat different correlation .

Fluorescence. The walls of spores and pollen (in common with plant cuticle, acritarchs, dinoflagellate cysts, and certain types of A . a . M . ) fluoresce in the visible spectrum when excited with ultraviolet light. Fluorescence colour (Fig. 2) varies both with organic matter composition and thermal maturity. The generation of these colours requires a sophisti­ cated microscope with an incident ultraviolet light

6 . 2 Practical Techniques S po re co l o u r

SCI

Co l o u r l e s s-pa l e ye l l ow

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Pa l e ye l l owl e m o n ye l l ow

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L e m o n ye l l ow

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A comparison of the Spore Colour Index (SCI) and Thermal Alteration Index (TAl) scales with verbal colour description . Vitrinite Reflectivity (Rv), Chitinozoan Reflectivity (Rch), spore fluorescence colours, and spectra are also included . The latter are measured over the range 400 - 700 nm and normalized to the same relative intensity. (From Otterjahn et al. 1974; Fisher et al. 1980; Smith 1983 . )

D u ra t i o n of h e at i n g

( 1 06 yrs)

A Karweil type diagram from which maximum palaeotemperature can be determined from a known spore colour (SCI only) with an estimated duration of heatinglburial. (From Cooper 1978 . )

Fig. 3

Fig. 2

source and dichroic beam splitters . The colours are difficult to estimate (in comparison to spore colours in white light) as they are pastel shades and rather faint. Colour can also be quantified with a photometer/monochrometer that generates a curve relating intensity -wavelength (nm), for which the maximum peak height, width, and position change with maturity (Fig. 2) . Quantitative fluorescence measurements are complicated by additional factors, such as intensity fading, microscope correc­ tions, and uncertainty over absolute standards . The Table

technique is therefore only employed in specialist laboratories .

Conodonts Conodonts have proved a popular group for deter­ mination of rank in Palaeozoic rocks due' to the widespread adoption of a single colour scale and the availability of standards . The conodont alteration index (CAI) is an eight-point scale (Fig. 4) that covers the temperature range < 50° to > 700°C . It is thus applicable to the widest range of maturity, including schists, although above CAI 6 difficulties occur in the event of hydrothermal alteration . The essential difference between conodonts and other microfos­ sils used in organic maturation studies is that cono­ donts are composed of a phosphatic mineral, with only trace amounts of organic matter. The initial colour changes (1 -5) result from maturation of this

1 Use of fossils as indicators of organic maturity. Microfossil group

Reflectivity

Spores Pollen Acritarchs Dinoflagellate cysts Chitinozoans Conodonts Vitrinite Note :

*

=

minor application;

Colour

Fluorescence

Geological range

***

**

***

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Silurian - Recent Devonian - Recent Precambrian - sub-Recent Triassic- Recent Ordovician - Devonian Cambrian-Triassic Silurian - Recent

*

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significant use .

6 Infrastructure of Palaeobiology

514

material, whilst above CAI 6 the mineral itself re­ crystallizes with oxidation of the organic matter and becomes clear. The phosphatic composition generally restricts their recovery to carbonate rocks and low rank shales, whilst the trace amount of organic matter limits the colour changes so only two CAI points are available within the oil window . Like all colour scales it is a series of points imposed on a continuous colour series and difficult to express in words, so standards are required for serious work.

Acritarchs Acritarchs, like pollen and spores, undergo changes in wall colour with increasing maturity. They have not been as widely used because the colour changes are more subtle and difficult to determine on the thinner walled tests, whilst thicker walled forms are frequently pigmented with significant natural colour. Consequently, where their geological ranges overlap, pollen and spores are used in preference to acritarchs . In the Lower Palaeozoic, where spores and vitrinite are largely absent, acritarch colour (and fluorescence) become important (although conodont colour is also available for this interval) . An acritarch colour alteration index has been produced (Fig . 4), with a five point scale based on colour changes in simple leiospheres . CAI

Te m p . r a n g e (QC)

1

<50-80

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Chitinozoans Polished sections through chitinozoan walls show reflectivity properties similar to the vitrinite maceral (a calibration is given in Fig . 2) . Usage is still only at an initial stage but chitinozoans should provide early Palaeozoic researchers with a quantitative scale as precise as that of vitrinite . Chitinozoans have the advantage of being large and thus easily measured in comparison to acritarch walls; they can also be recovered from every type of sediment within which they occur, unlike conodonts . Prob­ lems with low numbers in polished whole-rock preparations can be solved by using polished thin sections .

Other microfossil indicators of thermal maturity Kerogen components, such as dinoflagellate cysts, plant cuticle, and most types of A . O . M . , generally show colour and fluorescence changes with increas­ ing rank in a similar way to spores and pollen, although changes relate differently to temperature . For various reasons they have not become estab­ lished as routine thermal maturity indicators but can be used if required, and related approximately to the major points of existing scales . Situations where they are used include A . O .M . rich or distal

Acritarch co l o u r

Hyd roca r b o n g e n e ration

T ra n s l u ce n tl i ght ye l l ow

I m matu re

L i g h t ye l l owp a l e ye l l ow Pa l e ye l l owo range O ra n ged a r k b rown

-- - - - -

O i l & wet gas

1- - - - - - - Black

-

D ry gas

--------

Correlation of conodont colour and acritarch colour with verbal colour descriptions, temperature ranges, and the main zones of hydrocarbon generation . (From Legal! et al. 198 1 ; Rejebian et al . 1987, by permission of the Geological Society of America . )

Fig. 4

6 . 3 Museology oxic marine kerogen facies which may either lack a terrestrial input, with no spores, pollen, or vitrinite, or have had it diagenetically modified and/or diluted .

References Bostick, N . H . , Cashman, S . M . , McCulloh, T.H. & Wad dell, CT. 1979 . Gradients of vitrinite reflectance and present temperature in the Los Angeles and Ventura Basins, Cali­ fornia . In: D.F. Oltz (ed . ) Low temperature metamorphism of kerogen and clay minerals, pp . 65 -96. Society of Economic Paleontologists and Mineralogists (Pacific Section), Los Angeles, Ca. Cooper, B.5. 1978 . Estimation of the maximum temperatures attained in sedimentary rocks . In: G . D . Hobson (ed . ) Developments in petroleum geology Vo!. 1 . Applied Science Publishers, London . Epstein, A . G . , Epstein, J.B. & Harris, L.D. 1977. Conodont colour alternation - an index to organic metamorphism . U.5. Geological Survey, Professional Paper, No . 995 . Fisher, M.J., Barnard, P . C & Cooper, B . 5 . 1980 . Organic maturation and hydrocarbon generation in the Mesozoic sediments of the Sverdrup Basin, Arctic Canada. Pro­ ceedings of the Fourth International Palynological Conference, Lucknow (1 976 - 77) 2, 581 -588.

515

Heroux, Y., Chagnon, A . & Bertrand, R. 1979 . Compilation and correlation of major thermal maturation indicators. Bulletin of the American Association of Petroleum Geologists 63, 2128-2144. Legall, F . D . , Barnes, CR. & MacQueen, R.W. 198 1 . Thermal maturation, burial history and hotspot development, Paleozoic strata of southern Ontario- Quebec, from conodont and acritarch colour alteration studies. Bulletin of Canadian Petroleum Geology 29, 492 -539 . Otterjahn, K . , Teichmuller, M. & Wolf, M. 1974. Spectral fluorescence measurements of sporinite in reflected light, a microscopical method for the determination of rank in low rank coals . Fortschrifte in der Geologie von Rheinland und Wesifalen 24, 1 -36. Rejebian, V.A., Harris, A.G. & Heubner, J.5. 1987. Conodont colour and textural alteration: an index to regional meta­ morphism, contact metamorphism, and hydrothermal al­ teration . Bulletin of the Geological Society of America 99, 471 -479 . Smith, P . M . R . 1983 . Spectral correlation o f spore colouration standards . In: J. Brooks (ed . ) Petroleum geochemistry and exploration of Europe, pp. 289 -294. Special Publication of the Geological Society of London, No. 12. Staplin, F . L . , Dow, W . G . , Milner, CW.D., O' Connor, 0 . 1 . , Pocock, S.A.J . , van Gijzel, P . , Welte, D.H. & Yukier, M.A. 1982. How to assess maturation and paleotemperatures. Society of Economic Paleontologists and Mineralogists, Short Course No . 7.

6 . 3 Museology

6 . 3 . 1 Collection Care and Status Material P . R . CROWTHER

logical ordering of specimens enables material to be found as required, often without recourse to a man­ ual index or computerized documentation system (Section 6 . 3 . 2) .

Storage environment Introduction The fundamental aim of good fossil storage is to ensure the long-term survival of specimens, thus guaranteeing their future availability for study and display . The clean, ordered storage of specimens in a controlled environment is the physical basis of a good collection (Brunton et al. 1985; Rickards in Bassett 1979) . The ability to view and handle fossils easily, the use of appropriate containers, and the

Storage areas should be as free as possible from fluctuations in temperature and relative humidity (r. h . ) . Extremes and rapid changes of r . h . are the most common cause of damage to fossil material in museums. The vulnerability to oxidation of pyri­ tized fossils and pyrite-bearing matrices ('Pyrite Disease') increases to unacceptable levels when r . h . rises above about 55% . Neutralization o f affected material (Cornish in Crowther & Collins 1987) is no protection against future damage, which can

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only be prevented by keeping r . h . down. On the other hand, subfossil bone and some shale matrices shrink and crack when r.h. falls below about 45% . Rapid fluctuations of r . h . causes some clays and shales to swell and shrink alternately, leading to deterioration and loss. Monitoring and control of r . h . is therefore essential in geology storage areas, to keep conditions at 50 ± 5% r . h . This is achiev­ able either through full air conditioning or, more economically, through the use of portable de­ humidification and humidification equipment . Conditioned silica gel can maintain small, sealed volumes (storage boxes or display cases) at whatever r . h . is required. Temperature variation alone has little detrimental effect on fossil material, but because temperature is so intimately associated with r.h. (a fall in tempera­ ture causes r.h. to rise, and vice versa), its stabiliz­ ation is essential for r.h. control . A combination of high r . h . and high temperature accelerates the hydrolysis of hemicellulose to acetic acid in the wood of oak or birch ply cabinets; this may attack calcareous fossils and matrices (the so-called 'Bynes Disease') and such woods are best avoided for cabinet construction. Airborne dust is a particular and obvious menace to collections . It makes material difficult to examine and its removal is both time consuming and poten­ tially damaging to fragile specimens . Dust proofing can be incorporated at several levels within a quality storage system: individual storage trays can be made deep enough to support acetate tops; storage drawers and boxes should have tightly fitting lids; and the mobile bays in a compactable racking system can be edged with seals which mesh together when picking aisles are fully closed.

Storage furniture The ordered physical storage of fossils in a controlled environment cannot be realized cheaply . The specialized storage requirements of 'difficult' cat­ egories of specimens dictate particular solutions, e . g . large vertebrates (Brunton et al. 1985; Gentry in Bassett 1979) . Inside more generalized storage units, specimens should sit in paper-lined card trays (made of acid-free materials) to prevent abrasion and mixing . Storage unit design should be flexible regarding the use of drawers or shelves, and in the variety of drawer or shelf depths . They should in­ corporate good dust seals . Wooden cabinets are preferable (but not oak or birch ply for the reason given above) since they buffer against changes in

r.h. and cushion vibration. Mobile, rail-mounted, compactable racking systems make the most effec­ tive use of limited space, but they require strong floors and inevitably subject their contents to more vibration.

Status material Article n(g) of the 1985 International Code of Zoological Nomenclature (see Section 5 . 1 . 1) states that name-bearing types (holotypes, syntypes, lec­ totypes, and neotypes) are international standards of reference and are held in trust for science by those responsible for their safe keeping. Insti­ tutional responsibility in this regard is set out in the Code's Recommendation nG as follows : Every institution in which name-bearing types are deposited should : 1 Ensure that all are clearly marked so that they will be unmistakably recognized as name-bearing types . 2 Take all necessary steps for their safe pres­ ervation . 3 Make them accessible for study. 4 Publish lists of name-bearing types in its possession or custody. 5 So far as possible, communicate information concerning name-bearing types when requested . Failure to heed this code of practice hinders the progress of science and puts type material at risk. Any museum holding fossil type material should have a geologist on its permanent establishment; any university department or museum with types but no designated curator should deposit them elsewhere (Owen 1964) . It is the responsibility of the name giver to ensure that types go to an appro­ priate repository, and it follows that editors must insist on authors carrying out this duty as a con­ dition of publication . Indeed, taxonomic practice would be greatly enhanced if all status material (type, figured, and referred specimens) had to be registered in an appropriate institution as a condition of publication . The question of how best to store status material has provoked some disagreement (Brunton et al. 1985, p . C25) . Arguments that favour separating status material from the main collections include : meeting the ICZN and ICBN requirements regard­ ing type specimen care; convenience of access; increasing its physical security in better quality storage by improving protection from theft and damage from fire, flood, etc . ; and ease of evacuation in emergencies . Disadvantages of isolating such

6 . 3 Museology material include the risk that users might overlook its existence when working through the main col­ lection; and that it might be totally destroyed in the event of a disaster affecting that one particular part of the store . Whether type material should remain in its country of origin is another vexed question, although the ability of the home country to properly house and curate such material must be a primary consideration . Practices differ from nation to nation : Canada has legislation to ensure that types erected on Canadian material taken abroad for study are eventually repatriated; the Palaeontological Museum, Oslo, functions in effect as the National Museum for Norway and preferred policy is for all Norwegian primary type material to be held there (Bruton in Bassett 1979) ; the British Museum (Natural History) regards its holdings as inter­ national in scope, and considers it essential that related collections from different parts of the world are kept together, because palaeontology is a com­ parative science (see comment by Ball in Bassett 1979, p. 147) . Publication of a museum' s holdings of status specimens should be given high priority, since the dissemination of such information to the world at large is one of the important responsibilities that goes with being a type repository . Many of the larger museums can utilize an in-house publication for this purpose (Section 6.4), while smaller repositories can still fulfil their obligations to the wider scientific community via specialist journals such as the Geological Curator.

References Bassett, M . G . 1975 . Bibliography and index of catalogues of type, figured, and cited fossils in museums in Britain. Palaeontology 18, 753- 773 . Bassett, M . G . (ed . ) 1979 . Curation of palaeontological collec­ tions . Special Papers in Palaeontology, No . 22. Brunton, C H . C , Besterman, T . P . & Cooper, J.A. 1985 . Guidelines for the curation of geological materials . Miscellaneous Paper of the Geological Society, No. 17. Crowther, P.R. & Collins, CJ. (eds . ) 1987. The conservation of geological materiaL Geological Curator 4, 375 -474. Owen, D . E . 1964. Care of type specimens . Museums Journal 63, 288-291 Torrens, H . 5 . 1974. Palaeontological type specimens. Newsletter of the Geological Curators ' Group 1, 32 -35 .

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6 . 3 . 2 Collection Management and Documentation Systems P . R . C ROWTHER

Introduction All science depends on being able to 'repeat the experiment', to check the data on which conclusions drawn by others were based . In whatever way the fields of palaeobiology, biostratigraphy, taxonomy, evolutionary studies, etc. are delineated, each relies to a greater or lesser extent on our interpretation of the fossil record . It follows that fossil collections and their associated data represent the primary material evidence that underpins the intellectual structure of these elements of Earth science . The survival and availability of such collections is crucial to the ad­ vancement of knowledge, so that past results can be checked and new observational and analytical tech­ niques can be applied . Without museum collections, palaeobiology could not exist. The management of museum collections concerns the accessioning, control, cataloguing, use, and dis­ posal of specimens . The accelerating awareness of the importance of collections management has been triggered by: pressures on museums to demonstrate accountability for their collections; modern security and audit requirements; and the higher standards of inventory control expected by governing author­ ities (Roberts 1988) . Effective documentation is the key to collections management and is essential if the legitimate aspirations of museum users are to be met.

Information storage and retrieval A fossil without certain basic information (locality, stratigraphy, collector, etc.) is of little scientific value, however visually attractive it may be . Conversely, the most unprepossessing fossil fragment can con­ tinue to provide answers to new questions if it was effectively documented at the outset. A precise re­ cord of where, when, and how such a fossil was collected, and by whom, guarantees its future utility . All serious collectors have an obligation to science to ensure the long-term survival of their fossil material - which may represent an irreplaceable resource from a temporary exposure, and was per­ haps collected at great public expense from a remote part of the globe .

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6 Infrastructure of Palaeobiology

The principle of being able to repeat an obser­ vation is as axiomatic to the large numbers of speci­ mens associated with biometrics, population dynamics or phylogenetics as it is to the holotype concept in taxonomy . Today's collectorlresearcher can ensure the continued availability of primary source material - be it a unique type specimen or the thousands of measured specimens in a statistical study - by : 1 Allocating a unique identifying number to each specimen at the earliest opportunity. 2 Securely recording certain essential data about the specimen (locality, stratigraphy, collector name, collection date) and keying such a record to the specimen via its unique identifier. 3 Greatly improving the specimen' s chances of sur­ vival and long-term availability for future study by depositing it in an appropriately staffed and funded museum . This procedure ensures that the specimen's latent scientific potential is protected . The additional benefits that follow from producing specimen labels, classified catalogues, indexes (by donor, locality, age, etc . ) are many, and certainly make a collection more accessible to the user. But they can all be created later as required, manually or by computer, if the essential collection data has been properly recorded. Museum collections are assemblages of facts in the form of specimens, specimen-related data (Light et al. 1986), and (increasingly) site-related data (Raup et al. 1987; Crowther & Wimbledon 1988) . Many of these facts are available nowhere else; in the museum they remain available for re­ examination, reinterpretation, and restructuring, over and over again (Waters ton in Bassett 1979) . The physical well-being of collections (Section 6 . 3 . 1 ) and the dissemination o f information relating to those collections are both fundamental to the role of museums in Earth science today . An effective documentation system is the key to fulfilling such a role . The theory of how best to permanently link a specimen with its essential data is well established in museology, using a unique number and a secure register of sequentially ordered data entries . Unfor­ tunately, museum performance in this area has often left much to be desired, either through curatorial incompetence or (more usually) through under­ staffing and the tug of conflicting priorities . The efficient retrieval of specimen data i n a form capable of satisfying the needs of all museum users has proved an intractable problem. The traditional, manual approach is to maintain alongside the main

register as many running card indexes (by taxon, locality, age, donor, etc . ) as staff time allows. Any collection is to some extent 'self indexing' through the classified storage strategy adopted - by taxo­ nomic group, stratigraphical division, geographical location, or (more likely) by a combination of these . But in reality many museums are unable to keep pace even with basic registration of specimens, and it is very rarely possible to resource a fully effective manual system.

Computerized documentation systems Computing techniques are having a major impact on both the scale and type of problems being at­ tacked within contemporary palaeobiology (Sec­ tion 6 . 1 ) . Museums were quick to appreciate the potential of computer-based information techno­ logy for the sorting and selective retrieval of specimen-related data. Any conceivable index can be generated from a single input of specimen data, and interactive retrieval can be used to interrogate the database directly. Some museums with access to mainframe computers, either in-house or through computer bureaux, now have more than 15 years of experience to draw upon . The more recent devel­ opment of the desk-top microcomputer, with its increasingly more powerful data-processing abili­ ties and data storage capacity, has opened up the same advantages to a much wider spectrum of potential users . The sophisticated inputting, sorting, batch, and interactive retrieval routines that characterized the mainframe software packages of the nineteen-seventies can now be duplicated on a micro, while the storage capacity of hard discs enables typically lengthy museum specimen records to be held in sufficient numbers to cater for large collections . The availability of powerful relational database packages for microcomputers opens up exciting possibilities for the interactive interrogation of large complex files on low-cost hardware, in a way that would have seemed impossible just a few years ago . The capacity of the newest optical storage media makes it likely that within a very short time storage will cease to be any kind of limiting factor, even for the very largest collections . The effectiveness of computerized information retrieval has had additional benefits on the way museums deal with specimen-related data. The in­ formation must be structured in a standard form before inputting, and the terminology applied to

6 . 3 Museology different data categories must be rigidly controlled if sorting procedures are to produce useful output. This inflicts higher standards of data recording on museums than has traditionally been the case . Taken to its logical extreme, the adoption of a single data standard by museums, combined with an agreed thesaurus for terminology control, opens up the exciting prospect of combining museum databases and of their remote interrogation by users . How­ ever, there is as yet little international agreement about the structuring of museum data, and the question of terminology control is at an even more rudimentary stage . The V.K. is probably as far advanced as any other country in this regard, with the Museum Data Standard of the Museum Docu­ mentation Association (MDA) now in widespread use by museums, whether they employ the MDA's manual recording cards and/or supporting software packages or choose to develop in-house applications of commercial database packages . Full computerization o f specimen records entails a massive short-term commitment of data preparation time, since it obviously involves keying in all the manual records accumulated during a museum's history. Crucially, it also entails structuring the data and terminology to conform with agreed standards - and rigorously checking the data input. This is beyond the staffing resources of most museums, and computerization is commonly restricted initially to upgrading inventories; detailed computer catalogu­ ing is often limited to new material entering the museum . Nevertheless, the automatic scanning of manual records using developments of the 'optical character readers' already available open up the exciting possibility of direct input of typed or even handwritten records to a computer database, thereby drastically reducing data preparation time . At a time when museums are coming under in­ creasing pressure to make their reserve collections more accessible, new technology has an important role to play. As the efficient management of large taxonomic collections in the public domain becomes increasingly expensive, those responsible for such collections must become more adept at justifying their unique role to those who ultimately pay the cost through taxes or entrance charges . A database compiled for basic collections management pur­ poses can be made available to the general visitor via interactive terminals, after only minor modifications to strip out sensitive information (donor address, insurance value, storage location, etc . ) . Linked to a video disc (which are already capable of holding 50 000 images), such a system could provide instant

519

visual access on demand to a collection, yet involve no physical risk to the specimens themselves .

References Bassett, M . G . (ed . ) 1979 . Curation of palaeontological collec­ tions. Special Papers in Palaeontology, No . 22. Brunton, C . H . C . , Besterman, T.P. & Cooper, J.A. 1985 . Guidelines for the curation of geological materials . Miscellaneous Paper of the Geological Society, No . 17. Crowther, P.R. & Wimbledon, W.A. (eds) 1988 . The use and conservation of palaeontological sites. Special Papers in Palaeontology, No. 40. Light, R. B . , Roberts, D.A. & Stewart, J.D. (eds) 1986 . Museum documentation systems . Butterworths, London. Raup, D . M . , Black, c . c . , Blackstone, S., Dole H., Grogan, S . , Larsen . , P . , Jenkins, F., Pojeta, J . , Robinson, P . , Roybal, c . , Schopf, J.W., Stehli, F . G . & Wolberg, O . 1987. Palaeontological collecting. National Academy Press, Washington, DC. Roberts, D.A. (ed . ) 1988 . Collections management for museums. Museum Documentation Association, Cambridge, U.K.

6 . 3 . 3 Exhibit Strategies R . S . MILES

Introduction The purpose of mounting exhibits is normally to communicate information, so this section looks at some of the principles behind successful distance communication . By distance communication we imply the existence of a gap, either in time or space, between the sender and receiver of a message . This mode of communication applies typically to exhibits, whether comprising single posters or en­ tire museums . Classroom teaching, lectures and demonstrations, on the other hand, involve face-to­ face communication, in which the sender is there in person. It is important to distinguish between these two modes of communication, because if the sender is not there to answer questions, an effort must be made, at the stage of designing the communication, to ensure that it is intelligible to its intended audi­ ence . Good communication is selected for a purpose, and has a sound logical structure . Successful com­ municators know their audience, and attend both to the content ('what to say') and the form ('how to say it') of their communications .

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6 Infrastructure of Palaeobiology

The audience The organizers of exhibits inevitably form a mental image of their audience . Ideally this is based on hard data, e . g . the audience's vocabulary, under­ standing, interest in the subject, and commitment to its study. Care must be taken to avoid creating a false image, either through professional self-interest or limited experience of the audience . Where suf­ ficient data are not available, survey techniques similar to those found in market research can be used . Questionnaire design and sampling methods have been described by Loomis (1987) and Miles et al. (1988) . Accurate knowledge of the audience helps the communicator to connect his or her message with the viewer's world, and use language that is matched to the viewer's requirements . It is also helpful to know about the audience' s misunder­ standings (or 'alternative conceptions'), for these may need to be removed before the desired in­ formation can be imparted . For example, an intuit­ ively held Lamarckian view of evolution might block understanding of Darwin's theory of natural selection.

Selection and structure of content What to communicate, where to start, and how to continue? - in other words, the selection and order­ ing of the content - are basic questions in organiz­ ing any exhibit . Generally, there is more to say about a subject than the space or other resources allow, or the viewer's stamina permits, and there has to be some selection . The basis of this selec­ tion is a clear statement of purpose . For a group of exhibits this statement takes the form, at the broadest level, of a series of aims . But a more detailed statement of purpose is required for individual exhibits, and this is best provided by listing the teaching points, i . e . the facts, concepts, relationships, procedures, and so on that need to be communi­ cated . Teaching points generally divide into key concepts and ancillary points . Thus some are in­ cluded simply in order to define other concepts or to remove misconceptions, others to ensure the positive transfer of knowledge . Teaching points also help to promote clear communication among those responsible for exhibits, and provide a basis for judging the success of exhibits as pieces of communication (below) . The ordering or sequencing of content is done with the help of a strong central theme, to give a good flow of ideas and a framework that unifies the

facts, theories, and so on that are spelled out in the teaching points . It is important to tell only one story at a time; to organize things so that the audience knows what is going on (e . g . where they are going and how long it will take to get there); and to make the status of each message clear (e . g . is it the main conclusion or a supporting argument, is it a question or an instruction?) . A common way of ordering ideas is to place them in a logical sequence, e . g . concept A is dealt with before concept B because concept A must be under­ stood before concept B can be understood . However, it is often unwise to argue from first principles in exhibitions for the lay public, because of the need to attract and keep the viewer's interest and connect the message to his or her familiar world . Thus, if no particular sequence of concepts can be chosen on grounds of logical relations, it might still be better to deal with concept A before concept B, because on psychological grounds it is easier for the viewer to understand concept A before concept B (Fig. 1 ) . T o help the audience know what i s going o n it should be told, in an introductory exhibit, what the exhibits are about and how they are organized . In large exhibitions it may be necessary to repeat such information in different places. In addition to con­ ceptual orientation, it may also be necessary to provide topographic orientation, i . e . signposts, maps, and exhibit numbers . The aim is to indicate the correct route through the exhibits, and such orientation devices must be designed to make sense to viewers who have no prior understanding of the content and arrangement of the exhibits (Miles et al. 1988) .

Selection of media Communications media are the physical means of transporting messages from the sender to the re­ ceivers . Some media are normally used in the static mode, e . g . three-dimensional objects, graphics, and text; others are used in the dynamic mode and undergo a change of state during operation, e . g . audiovisuals and interactive computers . Selecting the appropriate medium for a particular message is important, yet never easy . There are few rules to assist the selection procedure, and the assessment of setting-up and maintenance costs is likely to weigh as heavily as educational advantage . If an exhibit is to communicate change over time or movement (e . g . continental drift), it is useful to use a dynamic medium, possibly a film or working model. But the basic exhibit media still remain

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objects (real things, replicas, and models), graphics (illustrations, diagrams, and photographs), and text (text panels and labels), and these are often used in combination . Although traditional, these media nevertheless require skill and care if they are to be used effectively . Lighting, conservation (e . g . certain fossils decay if conditions exceed 60% relative hu­ midity; print fades under ultraviolet rays), the selec­ tion of type and line lengths, and the integration of different media so that they work together, are just some of the things that have to be considered. For further information on all aspects of design, see Screven (1986), Hall (1987), and Miles et al. (1988) . Static object-cum-graphics exhibits elicit a rela­ tively passive response from viewers, who are simply asked to look and read . However, education­ alists have long understood that actively engaged learners are more likely to be successful than passive learners, which has led to the development of 'hands-on' exhibits that involve viewers in some sort of physical activity . This may be as simple as handling specimens, or as complex as operating interactive videodiscs . With larger exhibitions the more modern, dynamic media also give variety to the exhibits, which serves to maintain the viewers' interest. One caveat here : it is normally a good idea to employ professional help with complex media such as audiovisuals and computers . Such media

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are difficult to use well, and the exhibits are expens­ ive to set up and maintain .

Testing It is difficult for the distance communicator to be sure that a message will be clearly understood with­ out further explanation . Exhibit organizers who check on the effectiveness of their displays are often surprised at the variety of interpretations put on apparently simple and straightforward messages. The causes are to be sought in viewers' alternative conceptions, the different meanings attached to words, and the false perception of objects and graphics . The need to know the audience has been mentioned above; a further important way of lessen­ ing the chance of being misunderstood is to put exhibits through a process of developmental testing (also called formative evaluation) . The recommended procedure is called cued testing. Rough mock-ups of the exhibits are made . These may be handwritten, and photographs or drawings can often substitute for three-dimensional objects (Fig . 2) . The mock-ups are then tried out on small samples of the intended audience (ten people are generally sufficient) with the help of a simple ques­ tionnaire . Designs can be quickly adjusted and the procedure repeated until satisfactory results are ob­ tained. This is a qualitative approach involving no

6 Infrastructure of Palaeobiology

522

difficult statistics, and its worth has been demon­ strated over and over again with a variety of audi­ ences and institutions . For further information on the procedure, and for examples of questions used in testing, see Jarrett (1986) . Broader aspects of evaluation, including the summative evaluation of completed exhibitions, have been covered by Loomis ( 19 87) and Miles et al. ( 19 88) .

References Hall, M . 1987. On display. A design grammar for museum exhibitions . Lund Humphries, London . Jarrett, J . E . 1986 . Learning from developmental testing of exhibits . Curator 29, 295 -306. Loomis, R.J. 1987. Museum visitor evaluation: new tool for management. American Association of State and Local History, Nashville, TN . Miles, R . S . , Alt, M . B . , Gosling, D . C . , Lewis, B . N . & Tout, A.F. 1988. The design of educational exhibits, 2nd edn. Alien & Unwin, London . Screven, c . G . 1986 . Exhibitions and information centres : some principles and approaches . Curator 29, 109 - 137.

6.4 Societies, Organizations, Journals, and Collections J . NUDDS & D . PALMER

International bodies There are two international bodies whose areas of interest serve to link palaeobiologists world-wide .

International Union of Geological Sciences (lUGS) . This is one of the three largest scientific unions in the world . It was founded in 1961 to facilitate inter­ national co-operation in geology and is affiliated directly to UNESCO . Much of its work is concerned with the establishment of international com­ missions and committees on various branches of geology, e . g . Commission on Stratigraphy (see Sec­ tion 5 . 8), Committee on Geology Teaching, and its membership is composed mainly of international associations . There is, however, no commission on palaeontology, although the International Palae­ ontological Association (see below) is affiliated to the lUGS. Episodes, which replaced the Geological Newsletter in 1978, is the official organ of the lUGS .

International Palaeontological Association (IPA) . This is the major international organization linking palaeontologists throughout the world . Originally titled the International Palaeontological Union (IPU), it was formed in 1933 in Washington, D . C , at the Sixteenth International Geological Congress, its aim being the collaboration and co-operation of

international activity in palaeontology and stratigra­ phy . Membership was open to both societies and individuals . On becoming affiliated to the lUGS in 1966, the IPU was required to alter its name from 'Union' to 'Association', although this was not formalized until 1972 . Much of the IPA's activity is devoted to fostering smaller research groups (e .g. International Associ­ ation for the Study of Fossil Cnidaria, Graptolite Working Group, etc . ) and providing a forum for international co-operation between them (for list see Teichert & Yochelson 1985) . The IPA also co­ sponsors relevant meetings and is currently com­ posed of some 22 societies and nearly 500 individual members . Lethaia is its official organ (see below) .

Societies and organizations There are over 500 extant geoscience organizations according to a directory published in Geotimes (1987, 32(10); annually updated); some 30 or more are solely palaeontological but these do include several small local societies . Listed below are those rela­ tively few international and major national palaeon­ tological organizations, with information on their publications, etc. Also appended to this chapter (Appendix 1) is a more extended list of contact

6 . 4 Societies, Organizations, Journals, and Collections addresses for a number of other palaeontological organizations world-wide . There are also many 'non-geological' societies whose interests and activities impinge upon palae­ ontology and result in meetings and publications of direct concern to the palaeontologist, e . g . the Linnean Society, the Systematics Association, the Royal Society of London, the Society of Economic Paleontologists and Mineralogists . Access to this literature is best gained through the standard Earth science and biological bibliographies, such as the Bibliography and Index of Geology and Biological

Abstracts . Association of Australasian Palaeontologists (AAP). This is a specialist group of the Geological Society of Australia and is responsible for a variety of publications . Its official journal is Alcheringa (see below), while the Memoir series (begun in 1983) have thus far been either thematic in nature or in honour of an Association member. The free annual newsletter, Nomen nudum, acquaints members with the activities of palaeontological colleagues through­ out Australasia . Members of the AAP, who must also be members (ordinary, associate, or student) of the Geological Society of Australia, receive Alche­ ringa at a reduced rate, while the Memoirs are indi­ vidually priced . Applications for membership should be made to: the Administrative Officer, Geological Society of Australia Inc ., 606 A.N.A. House, 301 George Street, Sydney, New South Wales 2000, Australia .

Palaeontological Association . Founded in 1957 to promote research in palaeontology, the Association is based in London, U.K., but has a world-wide membership which is open to individuals, insti­ tutions, libraries, etc. on payment of the appropriate annual subscription . Institutional membership is only available by direct application, not through agents, while student membership is open to per­ sons receiving full-time instruction at an institution recognized by Council . Applications for member­ ship should be made to: the Membership Treasurer, Dr. H.A. Armstrong, Department of Geological Sciences, The University, South Road, Durham DH1 3LE, U.K. The Association holds an Annual Conference in December, and organizes review seminars, lecture meetings, and field excursions throughout the year. It publishes the quarterly journal Palaeontology (see below) and a quarterly Newsletter, which are issued free to all members of the Association; and Special Papers in Palaeontology

523

(see below) .

Paleontological Society. Founded in 1908, the Pale­ ontological Society is based in the U . 5 . A . and pro­ duces a number of publications . Applications for membership should be made to the Secretary, Dr D . L . Wolberg, New Mexico Bureau of Mines, Socorro, NM 87801, U . S . A . All members receive the bi-monthly Journal of Paleontology (see below) and Memoirs of the Paleontological Society (see below) . Members may also receive the quarterly journal Paleobiology (see below) at a reduced subscription. (Paleobiology Subscriptions, P.O. Box 1897, 810 East 10th St., Lawrence, KS 66044, U.5.A.). The Society also publishes two series of topical publications: Short Course Notes are published each year as part of the University of Tennessee Studies in Geology Series, for distribution at the Society's annual short course, held with the Annual Meeting of the Geological Society of America; the Special Publications series includes the proceedings of symposia sponsored by the Society at its regional meetings . Both are avail­ able from The Paleontological Society, Department of Geological Sciences, University of Tennessee, Knoxville, TN 37996 - 1410, U . S . A .

Palaeontographical Society. Founded in 1847, the Society exists for the purpose of figuring and de­ scribing British fossils in its Monographs (see below) . Subscriptions are due on 1st January each year. Membership applications should be made to the Secretary, Mr S . P . Tunnicliff, British Geological Survey, Keyworth, Nottingham NG12 5GG, U.K. All members receive the Annual volume, which consists of a number of complete or part mono­ graphs . Members also receive 25% discount on all in-print and reprinted publications, and 33% dis­ count on micro-edition publications, which may be ordered through the Secretary.

British Micropalaeontological Society (BMS) . Founded in 1970, the Society's aim is to further the study of micropalaeontology. Meetings and demonstrations are held regularly throughout the year and the BMS now publishes a number of both serial and oc­ casional publications . Membership is open to individuals and to libraries on payment of the ap­ propriate annual subscription . Membership appli­ cations should be made to the Treasurer, Dr. I.P. Wilkinson, British Geological Survey, Keyworth, Nottingham NG12 5GG, U.K. Publications include the Journal of Micropalaeontology (see below) and

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The British Micropalaeontologist (a newsletter) which are issued free to all members; and A Stereo-Atlas of Ostracod Shells (see below) . Paleontological Research Institution (PRI) . Founded in 1932, the PRI is based in Ithaca, New York, and publishes two series of palaeontological mono­ graphs, Bulletins of American Paleontology and Palae­ ontographica Americana (see below) . These give authors a relatively inexpensive outlet for the publi­ cation of significant longer manuscripts . In addition, it reprints rare but important older works from the palaeontological literature . The PRI headquarters in New York houses a large collection of invertebrate type and figured specimens, an extensive collection of well documented fossil specimens, and a com­ prehensive palaeontological research library . For additional information contact Director, Dr W.D. Allmon, 1259 Trumansburg Road, Ithaca, New York 14850 - 1398, U . S . A .

Society of Vertebrate Paleontology (SVP) . Founded in 1941, membership of the U . S . A . based SVP is open to anyone 18 years of age or over who is interested in any aspect of fossil vertebrates . Applications for membership and all matters regarding subscriptions should be directed to the Secretary-Treasurer, Dr Robert M. Hunt Jr. , Division of Vertebrate Pale on­ tology, W436 Nebraska Hall, University of Nebraska, Lincoln, Nebraska 68588 -0514, U . 5 . A . The Society produces a News Bulletin and supports the Journal of Vertebrate Paleontology. Journals

Scientific literature of all kinds continues to grow enormously (Menard 1971), with current estimates of some 50 000 journals published world-wide . The quickest entree into this bibliographic 'ocean' is to first clarify exactly what is wanted, and then to ask a sympathetic and trained librarian for help . Failing this, the standard bibliographical procedure has to be followed, starting with bibliography of bibli­ ographies, such as Mackay (1973) . For current Earth science literature (especially in the English language) the monthly Bibliography and Index of Geology is most widely used and draws its data from nearly 3000 journals, plus books, etc . However, this and other major bibliographical sources are only available in specialist libraries . Fortunately, recent advances in library information technology have made such bibliographies available 'on line' e . g . GeoRef (see Hall & Brown 1987) .

Palaeontology is essentially a historical science with fossils as its raw material, and taxonomic pro­ cedure and zoological nomenclature as its means or code of conduct (see Section 5 . 1 ) . The fundamental principles or criteria by which this 'business' is conducted include the concept of the type specimen and type series (which has essentially to be suitably housed and conserved - safe and yet accessible; see Section 6 . 3 . 1) and the historical priority of authorship and description (provided it fulfils cer­ tain agreed standards of text, illustration, and publi­ cation, in order to promote stability and universality in the scientific naming of animals) . One of the main implications of this taxonomic prerequisite for palaeontology is that it requires an historically cumulative literature . Since the val­ idity of previously published nomenclature extends back by convention as far as 1757, the student potentially requires access to well over 200 years of published work. Many of the older sources are rare books or monographs and journals that had very limited editions and were not widely circulated (Thornton & Tully 1971 ; see also the journal Archives of Natural History, published by the Society for the History of Natural History) . This historical principle is characteristic of all the taxonomically­ based natural sciences but is not a feature of the physical sciences or many of the newer, rapidly growing and 'high profile' sub sciences (Menard 1971). In many of these areas literature over 25 years old is 'unshelved' and considered redundant. Only a 'core' of the most cited journals are regarded as important - about 4000 for the whole of science as far as the Science Citation Index is concerned, of which only 12 are purely palaeontological . The literature profile required for the study of palaeontology is fundamentally different. This is demonstrated by sample citations drawn from papers published in recent issues of the journals

Geologica et Palaeontologica, Journal of Paleontology, Palaeontology, and Paleobiology. A further sample of biological papers from the weekly interdisciplinary science journal Nature was taken for comparison. The citations from each journal were ordered histori­ cally and assembled to produce cumulative relative frequency curves (Fig. 1 ) . These clearly separate into two groups : one includes a significant pro­ portion of older work (10% pre-191O); the other cites very little nineteenth century or older work (less than 2% pre-1910) . The difference between the two patterns stems directly from the former group being primarily specimen oriented, i.e. taxonornically­ based work, which requires recognition of historical

6.4 •

•

Societies, Organizations, Journals, and Collections

Ceologica et Palaeon tologlca ( n = 467)

1 00 %

Pa laeontologv

(n

=

385 )

.. lournal of Pa leontology (n

o

298)

30%

Pa leobiology (n

o

=

=

358)

Na ture (n

=

121 ) 1 I I I 1 I 1 I 25 1 y e a r

1 0%

cut;
1 901

1 961

Fig. 1

Proportional cumulative curves (log-linear scale) of sample bibliographic citations from recent issues of five science journals, arranged historically.

priority. The latter group (Paleobiology and the Nature sample) includes little in the way of purely taxonomic work but rather documents more theor­ etical and thematic research . Nevertheless, this group still shows an indirect reliance on older literature through the frequent citation of work published in the former group . If a 25 year cut-off (i . e . all pre-1960) were to be imposed on access to the type of literature at present currently being used for research that is published in the more taxo­ nomically based journals, then at least 300/6 of the references would not be available . Another important aspect of the literature used in palaeontological research is the remarkable diversity of published sources required . A small survey of 500 references from the bibliographies of the nine papers in Palaeontology 30(4) (1987) consistently shows that, even with variable length citation lists (from 28- 100 in sample), 50% are derived from different journals and 20% are non-periodical publi­ cations, so that only 30% are repeated journal ci­ tations . Furthermore, each successive paper cites a

525

high proportion of different journals and only a small proportion of citations (10 - 20%) are common between any two or three papers . On a world-wide basis there are nearly 100 purely palaeontological current serial publications, which vary enormously in their scope, print runs, cost, etc. Of these, about 20 are mentioned in some detail below and a further 70 listed in a more limited way in Appendix 11 of this chapter, along with a further 17 bibliographical publications in Appendix Ill . Titles are listed in alphabetical order. The letter codes at the end of each citation in the following list refer to : A, the number of subscribers to the journal; B, the print run; C, the average number of pages per year; D, the page size; International Standard Serial Number (ISSN); and CODEN.

Alcheringa. This is the organ of the Association of Australasian Palaeontologists of the Geological Society of Australia (see above) . Issued twice yearly, it first appeared in 1975 and covers all aspects of palaeontology, including taxonomy, biostrati­ graphy, micropalaeontology, vertebrate palaeon­ tology, palaeobotany, palynology, palaeobiology, palaeoanatomy, palaeoecology, biostratinomy, bio­ geography, chronobiology, biogeochemistry, and ichnology. Review articles are welcomed and oc­ casionally a single volume is devoted to a particular topic. Emphasis is placed on high quality illus­ trations . Manuscripts are published approximate­ ly one year after acceptance and should be sent to Dr J.W. Pickett, Specialist Services Section, Geological Survey of New South Wales, Mineral Resources Development Laboratory, PO Box 76, Lidcombe, New South Wales 2141, Australia. Subscription information may be obtained from the Geological Society of Australia Inc. , 606 A . N . A . House, 301 George Street, Sydney, New South Wales 2000, Australia. Members of the As­ sociation of Australasian Palaeontologists receive Alcheringa at a reduced rate . The journal is abstracted in Current Contents, Geological Abstracts, GeoRej, Petroleum Abstracts, and Science Citation Index. A, 650; B, 1000; C, 344; D, 17 X 25 cm; ISSN, 031 1 - 5518; COD EN, ALCHDB .

Fossils and Strata. A sister journal to Lethaia (see below), it was first issued in 1972 and comprises an internationally distributed series of monographs and memoirs in palaeontology and stratigraphy. It is issued irregularly in Numbers; by the end of 1991 31 had appeared. While Lethaia is a fully inter­ national journal, Fossils and Strata provides an outlet

526

6 Infrastructure of Palaeobiology

for more comprehensive systematic and regional descriptions dealing with areas in the five countries of Norden, or written by palaeontologists and stra­ tigraphers from these countries . Contributions by colleagues in other countries may also be included as far as this series is deemed to be an appropriate medium . Articles can normally be accepted only if they are heavily subsidized by the national Research Council in their country of origin, or by other funds. Most papers are in English, but they may be in French or German. Manuscripts, which are pub­ lished approximately four to five months after acceptance, should be sent to S . Bengtson, Institute of Palaeontology, PO Box 558, S-75 122 Uppsala, Sweden . Issues are individually priced and may be ordered from the publishers, Universitetsforlaget, Postboks 2959, Toyen, Oslo 6, Norway. Members of the IPA (see above) are offered discount prices on all issues. The journal is abstracted in Biological Abstracts, British Geological Literature, Geological Abstracts, and

GeoRef. B, 1000; C, 124 (per number); D, A4; ISSN 0024 - 1 164 .

Geobios . Published with the cooperation o f the Centre National de la Recherche Scientifique, it first appeared in 1968 and is issued bi-monthly. It pub­ lishes papers of international interest on all aspects of palaeontology, stratigraphy, and palaeoecology. Articles may be in English or French. Manuscripts are published two to six months after acceptance and should be sent to Geobios, Centre des Sciences de la Terre, Universite Claude-Bernard, 27-43 Boulevard du 1 1 Novembre, 69622 Villeurbanne, France. Subscription information may be obtained from the Secretary at the above address . The journal is abstracted in Biological Abstracts, Bulletin

Signaletique, Pascal Folio, Current Contents, Geological Abstracts, GeoRef, Geoscience Database, and Refera­ tiunyi Zhurnal. X

Lahnberg, Germany. This journal is Abstracted in

Bibliography and Index of Geology, Pascal Folio, and Viniti I Moskva . A, 92; B, 600; C, 192; D, A4; ISSN 0072 - 1018; CODEN, GPALA2.

Journal of Micropalaeontology. The British Micro­ palaeontological Society (see above) published the first volume in 1982 and produces two issues per year. It carries papers on any aspect of micropalae­ ontological research, world-wide, and includes studies on Recent forms also. It tends to be domi­ nated by taxonomy and palaeoecology . Manuscripts are published from three months to one year after acceptance and should be sent to Dr M . C . Keen, Department of Geology, University of Glasgow, Lilybank Gardens, Glasgow G12 8QQ, U.K. The journal is issued free to all members of the Society (see above) . A , 800; B , 1000; C , 240; D , 2 1 x 27 cm; ISSN 0262 821X.

Journal of Paleontology. The main publication of the Paleontological Society (see above), it was first issued in 1927 and appears bi-monthly . All aspects of palaeontology are dealt with, but taxonomy, palaeoecology, biostratigraphy, and evolution tend to dominate . Papers are published approximately six months after acceptance and should be sent to Don C . Steinker, Department of Geology, Bowling Green State University, Bowling Green, OH 43403, U.S.A. The journal i s issued free t o all members o f the Paleontological Society (see above) and is abstrac­ ted in Biological Abstracts, Current Contents, British

Geological Literature, Geological Abstracts, GeoRef, Indian Science Review, Petroleum Abstracts, and Science Citalion Index. A, 2773; B, 3150; C, 1320; D, 21 . 5 x 28 cm (formerly 17.5 x 24 cm); ISSN 0022- 3360; CODEN, JPALAZ .

27 cm; ISSN

Journal of Vertebrate Paleontology. Founded in 1980

Geologica et Palaeontologica. Published in Marburg, it appears annually and was established in 1967 to publish articles on all aspects of geology and palaeontology from all over the world . Articles may be in either English, German, or French . Manu­ scripts are published about one year after acceptance and should be sent to Redaktion von Geologica et Palaeontologica, Fachbereich Geowissenschaften der Philipps-Universitat, D-3550 Marburg/Lahn,

(first issue 1981) at the University of Oklahoma, since 1984 it has been supported by the Society of Vertebrate Paleontology (see above) . Published quarterly, it accepts papers on all theoretical and applied aspects of the palaeontology of chordates, especially their origins, evolution, anatomy, tax­ onomy, biostratigraphy, palaeoecology, palaeoge­ ography, and palaeoanthropology . Manuscripts are published approximately 18 months after acceptance and should be sent to either Richard Cifelli, Oklahoma Museum of Natural History, University of Oklahoma,

A, 528; B, 650; C, 900 - 1000; D, 21 0016- 6995; COD EN, GEBSAJ .

6.4

Societies, Organizations, Journals, and Collections

Norman, Oklahoma 73019, U.5.A. (mammals) or Hans-Dieter Suess, Vertebrate Palaeontology, Royal Ontario Museum, Toronto, Canada M5S 2C6 (other vertebrates). The journal is issued free to all members of the Society of Vertebrate Pale ontology (see above) and is abstracted in Biological Abstracts and GeoRef. A, 1000; B, 1200; C, 400; D, 21 . 6 x 27. 9 cm; ISSN 0272-4634; CODEN, JVPADK.

Lethaia. The official organ of the IPA (see above) and sponsored by the National Councils for Scien­ tific Research in Denmark, Finland, Norway, and Sweden, Lethaia was first issued in 1968 and is published quarterly. It includes articles of inter­ national interest in palaeontology and stratigraphy. Articles on the morphology and anatomy of fossil plants and animals should be of general interest to palaeontologists, and articles on systematic palaeon­ tology should deal with the higher units in system­ atics or key forms on which concepts of classification are based. New features, new forms, and significant changes in the known distribution of fossil organ­ isms also constitute important criteria for the acceptance of articles . Palaeobiology, particularly palaeoecology, and ecostratigraphy are the core topics of the journal. Articles on stratigraphy should meet the same requirements for general interest and deal with stratigraphic principles, correlations of at least continental-wide importance, stratotype areas of key character, new occurrences or revisions which establish major features in palaeogeography, etc . Lethaia, with its sister journals Boreas and Fossils and Strata (see above), forms part of a publishing system with special ambitions to apply modern techniques in scientific publication . Most papers are in English, but they may be in French or German. Manuscripts are published approximately one year after acceptance and should be sent to the Editors of Lethaia, Department of Palaeozoology, Swedish Museum of Natural History, Box 50007, 5-104 05 Stockholm, Sweden. Subscription information may be obtained from the Norwegian University Press (Universitetsfor­ laget AS), PO Box 2959, Toyen, Oslo, Norway. The j ournal is abstracted in Biosciences Information

Service of Biological Abstracts, British Geological Literature, Current Contents, Geological Abstracts, GeoRef, Current Awareness in Biological Sciences, Con­ tributions to Coastal, Ocean, Lake and Waterway (CERE), and Science Citation Index. A, 1200; B, 1500; C, 384; D, 17 1 1 64; CODEN, LETHAT.

x

25 cm; ISSN 0024 -

527

Micropaleontology. Published by the Micropaleonto­ logy Press (American Museum of Natural History) since 1955, it appears quarterly and covers the stra­ tigraphy, systematics, morphology, palaeobi­ ology, and palaeoecology of all micro-organisms with hard parts . The journal is relevant to Earth sciences, oil exploration, and oceanography and is dominated by foraminiferans, ostracodes, radio­ larians, and nannoplankton. Manuscripts, which are published just 13 weeks after acceptance, should be sent to Dr J. Van Couvering, Micropaleontology Press, American Museum of Natural History, Central Park West at 79th Street, New York, NY 10024, U . S . A . Subscription information may b e obtained from Micropalaeontology Subscriptions, Dept. MPT, Box 3000, Denville, New Jersey 07834, U . S . A . The journal is abstracted in Biological Abstracts, Chemical Ab­

stracts, Geological Abstracts, GeoRef, Ocean Abstracts, Petroleum Abstracts, and Science Citation Index. There is also an irregular monograph series Micropaleon­ tology Special Publication (1976; ISSN 0160- 2071) and bibliographical series (see Ellis and Messina Catalogues below) . A, 1000; B, 1300; C, 388; D, 21 . 6 x 27. 9 cm; ISSN 0026- 2803; CODEN, MCPLAI

Palaeontographica. Published by E. Schweizer­ bart'sche Verlagsbuchhandlung of Stuttgart, this major international monograph series was initiated in 1846 . It is divided into two series, A and B, the former dealing with palaeozoology and strati­ graphy, the latter with palaeobotany. In both series five volumes (i. e . ten numbers) are produced every year. This journal has established a world-wide re­ putation for the highest standards of monographic treatment and accepts papers on all fossil groups of all ages. Papers may be in English, German, or French . Publication usually occurs within a year of acceptance and manuscripts for Series A should be sent to Prof. Dr W. Haas, Institute fur Palaontologie der Universitat, Nussallee 8, D-5300 Bonn 1, Ger­ many; for Series B send to Dr H. J . Schweitzer at the same address. Subscription information may be obtained from the publishers (see above) at Johannesstrasse 3A, D-7000 Stuttgart 1, Germany . The journal is ab­ stracted in Biological Abstracts, British Geological Literature, and GeoRef. C, 855; D, 23 x 29 cm; ISSN 0375 -0442 (Series A), 0375 - 0299 (Series B); CODEN, PGABA8(A), PABPAD(B) .

528

6 Infrastructure of Palaeobiology

Palaeontographical Society Monographs. Monographs of the Palaeontographical Society (see above) were first published in 1848 (for 1847) . Each annual volume consists of a number of complete or part Monographs . They are confined to descriptions of British fossils, restricted geographically, strati­ graphically, or taxonomically. The Palaeonto­ graphical Society sets very high standards for its monographs and the interval between acceptance of an offered title and publication may be many years . Manuscripts and should be sent to either Dr. J. Hutt, Edinvillie, Gartly, Huntly, Aberdeenshire AB5 4RS, u.K. or Or A.T. Thomas, Department of Geological Sciences, University of Birmingham, PO Box 363, Birmingham B15 2TT, U.K. The annual volume is issued free to all members of the Palaeontographical Society (see above) . Non­ members may purchase the publications of the Society at the listed prices from The Natural History Museum, Cromwell Road, London SW7 SBD, U.K. The journal is abstracted in Biological Abstracts, and

GeoRef.

A, 700- 750; B, 900; 0, approx. quarto; ISSN 0376 2734; CODEN, PLTSAJ.

Palaeontologica Sinica. Published by the Institute of Vertebrate Palaeontology and Palaeoanthropology, Academia Sinica and the Nanjing Institute of Geology and Palaeontology, Academia Sinica, this well established Chinese publication first appeared in 1922 . It is the major monograph series for China and two or three numbers appear annually, each being a single substantial paper. Systematic stud­ ies are often complemented by palaeoecological, palaeobiogeographical, and biostratigraphical stud­ ies of the relevant taxa, and palaeoanthropology, palaeozoology, and palaeobotany receive equal coverage . Papers are in Chinese with an English translation. They may take up to two years to be . published after acceptance and should be sent to the editor, Chang Mei-Li, Nanjing Institute of Geology and Palaeontology, Academia Sinica, Chi­ Ming-Ssu, Nanjing, People's Republic of China. The journal is abstracted in GeoRef. A, 1200; B, 2000; C, 250; 0, 19 X 26 cm; ISSN 0375 054X (Series A); 0375 - 0531 (New Series B ­ Invertebrates o f China), 0578 - 1 604 (Series C) .

Palaeontology. The journal of the Palaeontological Association (see above), it first appeared in 1957 and is issued quarterly. This widely-read inter­ national journal publishes papers on all aspects of palaeontology from all areas of the world and in-

cludes Recent material of palaeontological relevance . Review articles are particularly welcome, and short papers can be published rapidly . Preference is given to works of more than local significance . A high standard of illustration is a feature of the journal. Manuscripts, which are published one year to 18 months after acceptance, should be sent to Prof. D. Edwards, Department of Geology, University of Wales College of Cardiff, Cardiff CFl 3YE, U.K. The journal is issued free to all members of the Association (see above for details) and is abstracted in Biological Abstracts, GeoReJ, Science Citation Index, and GeoSciTech (online) . A, 1400; B, 2150; C, 785; 0, 19 x 24. 5 cm; ISSN 0031 -0239; CODEN, PONTAD .

Paliiontologische Zeitschrift. The official journal of Palaontologische Gesellschaft, it was first issued in 1914 and appears quarterly . Papers appear in English or German on all aspects of systematic palaeontology, palaeoecology, and palaeobioge­ ography. Manuscripts are published from nine months to one year after acceptance and should be sent to Or R. Werner, Forschungs-Institut Senckenberg, Senckenberganlage 25, 6000 Frankfurt am Main, Germany . The journal is abstracted in Biological Abstracts, British Geological Literature, and

GeoRef.

A; c. 1000; B, 1500; C, 350; 0, 16 0031 - 0220; CODEN, PAZEAW.

X

24 cm; ISSN

Paleobiology. This is a quarterly journal of the Paleontological Society (see above) which first appeared in 1975 and specializes in articles dealing with biological palaeontology. The emphasis is on biological or palaeobiological processes and pat­ terns, including speciation, extinction, development of individuals and of colonies, natural selection, evolution, and patterns of variation, abundance, and distribution in space and time . Papers concern­ ing Recent organisms are considered appropriate if they are of interest to palaeontologists . Taxonomic papers are welcome if they have broad applications . Book reviews can also b e submitted o r invited. Manuscripts should be sent to Paleobiology, Depart­ ment of Geology, University of Cincinnati, Cincinnati, OH 45221 , U.s.A. Although published by the Paleontological Society (see above), a subscription to Paleobiology is in addition to the Society's dues. The journal is abstracted in Biological Abstracts, Current Contents, GeoReJ, Petroleum Abstracts, and Science Citation

Index.

6 . 4 Societies, Organizations, Journals, and Collections B, 2500; C, 471 ; 0, 17.5 x 25. 5 cm; ISSN 0094-8373; CODEN, PALBBM .

Paleontological Journal. Published four times a year by Scripta Technica (a subsidiary of John Wiley & Sons), it first appeared in 1967. It consists of trans­ lations in English of papers from the Russian­ language journal Paleontologicheskiy zhurnal, pub­ lished by the U . S . 5 . R. Academy of Sciences . It deals with the anatomy, morphology, and taxonomy of extinct animals and plants, their phylogenetic re­ lationships, distribution, ecology, origin, and evol­ ution, as well as the biostratigraphy of Eastern Europe and Asia . Each issue consists of papers selected from one issue of Paleontologicheskiy zhurnal, and appears approximately 16 weeks after original publication . The editor is Matthew H. Nitecki, Geology Department, Field Museum of Natural History, Chicago, Illinois, U . S . A . Subscription information can b e obtained from the Paleontological Journal, Subscriptions Depart­ ment, John Wiley & Sons, 605 Third Avenue, New York, NY 10158, U . S . A . The journal is abstracted in Biological Abstracts and GeoRef. C, 562; 0, 18 x 25 . 5 cm; ISSN 0031 - 0301 (Russian version, 003 1 - 031X); COD EN, PJOUAK.

Palynology. Published by the American Association of Strati graphic Palynologists (AASP, founded 1967), it appeared in 1977 and is issued annually. Papers are published on all aspects of Quaternary or pre-Quaternary palynology from all over the world, but are dominated by contributions relating to North America. Each volume includes the proceed­ ings of the previous annual meeting. Manuscripts should be submitted to David K. Goodman, Arco Oil and Gas Co . , Research Centre, 2300 West PIano Parkway, PIano, Texas 75075, U . 5 . A . Palynology i s issued free t o all members o f the AASP; subscription information may be obtained from the Treasurer at the above address. An ir­ regular Contribution Series (ISSN 0160- 8843) and quarterly Newsletter (ISSN 0192 - 7299) are also published . The journal is abstracted in Biological

Abstracts, British Geological Literature, Geological Abstracts, GeoRef, and Petroleum Abstracts . C, 962; 0, 21 . 6

x

27. 9 cm; ISSN 0191 - 6122.

Pollen et Spores. Published with the co-operation of the Centre National de la Recherche Scientifique, it was first issued in 1959 and appeared quarterly until 1989 . It published papers on all aspects of

529

palynology on a world-wide basis, either in French or English . Subscription information BP 2015, 34024 Montpellier Cedex, France . The journal was abstrac­ ted in GeoRef. A, 400; B, 800; C, 600; 0, 15.5 x 24 cm; ISSN 0375 9636; CODEN, POSPAQ .

Review of Palaeobotany and Palynology. One of sev­

eral i�tern�tional geoscience journals published by Elsevler Saence Publishers, PO Box 211, 1000 A E, �msterdam, The Netherlands, it was first published In 1967, and there are eight issues a year . The main language is English but texts may also be submitted in French and German . The scope of the journal covers the whole of palaeobotany and palynology . Manuscripts should be sent to the Editorial Office Review of Palaeobotany and Palynology, P . O . Bo� 1930, 1000 BX Amsterdam, The Netherlands . The journal is abstracted in Biological Abstracts, British

Geological Literature, Current Contents, Geological Abstracts, GeoRef, Pascal Folio, Petroleum Abstracts, and Science Citation Index . ISSN 0034- 6667; CODEN, RPPYAX .

Revue de Micropaleontologie. First published in 1958, this French journal appears quarterly and accepts articles, congress and symposia reports, and book reviews dealing with any aspect of micropalaeon­ tology, especially taxonomy and stratigraphy . Articles may be in English, but are usually in French . Manuscripts are published from nine to 18 months after acceptance, and should be sent to Revue de Micropaleontologie, Maison de la Geologie, 79 Rue Cl . Bernard, 75005 Paris, France . Subscription information may be obtained from the same address. The journal is abstracted in British Geological Literature, GeoRef, Pascal Folio, and Pet­ roleum Abstracts .

A, 550; B, 700; C, 266; 0, 21 1598; CODEN, RMCPAM

x

27 cm; ISSN 0035 -

Museums

On a world-wide scale there are a great number of institutions which house palaeontological collec­ tions of importance . The directory World Palaeon­ tological Collections (Cleevely 1983) lists some 500 named collections, of which over 200 are in the U.K. Cleevely's invaluable work builds on several pre­ vious compilations and includes discussions on problems of compiling such directories, a brief history of earlier guides to geological collectors with

530

6

Infrastructure of Palaeobiology

brief bibliographies on the history of palaeontology, fossil collecting, collections and their published catalogues, and other relevant reference sources. Listed in Appendix IV are the main international and national museums with major fossil collections . Many important regional and university museums have had to be excluded and the reader is referred to Cleevely for a more complete listing. There is a bias towards British museums and Cleevely's geo­ graphical ordering has been followed .

References Cleevely, R.J. 1983 . World Palaeontological Collections, British Museum (Natural History) and Mansell Publishing, London . Hall, J . L . & Brown, M.J. 1987. On-line bibliographic databases (4th edn) . ASLIB, London. MacKay, J.W. 1973 . Sources of information for the literature of Geology. An introductory guide. Geological Society of London, Bath . Menard, H.W. 1971 . Science: growth and change. Harvard University Press, Cambridge, Ma . , Teichert, C . & Yochelson, E . L . 1985 . The International Palaeontological Association: historical perspective. Episodes 8, 252 �256 . Thornton, J . L . & Tully, R.I.J. 1971 . Scientific books, libraries, and collectors. A study of bibliography and the book trade in relation to science (3rd edn) and Supplement 1 969 � 75 (1978) . The Library Association, London .

Appendix I: Palaeontological organizations­ supplementary list American Association of Stratigraphic Palynologists . (Founded, 1967; membership, 400) G . D . Wood, Amoco Production Co. , PO Box 3092, Houston, TX . 77253, U.5.A. Publications : Palynology, Contribution Series, Newsletter. Asociacion Paleontologica Argentina. (Founded, 1955; membership, 400) Maipu 645, 1 Piso, Buenos Aires, Argentina. Publication: Ameghiniana. Association Paleontologique Fran<;aise . Laboratoire de Paleontologie, Museum National d'Histoire Naturelle, 8 rue Buffon, 75005 Paris, France . Austrian Paleontological Society (G sterreichische Palaontologische Gesellschaft) . (Founded 1966; member­ ship, 166) Institut fUr Palaontologie der Universitat, Universitatsstrasse 7/1 1, A-I01O Vienna, Austria. Publi­ cation: Beitriige zur Paliiontologie von Osterreich . Bernard Price Institute for Palaeontological Research . Univer­ sity of Witwatersrand, Johannesburg 2001, South Africa. Publication : Palaeontologia Africana. Botanical Society, Paleobotany Section . Gar W. Rothwell, Department of Botany, Ohio University, Athens, OH 45701, U.5.A. Publication: Bibliography of North American Paleobotany.

Cushman Foundation for Foraminiferal Research. Museum of Comparative Zoology, Invertebrate Paleontology, Harvard University, 26 Oxford Street, Cambridge, MA 02138, U.5.A. Publications: Journal of Foraminiferal Research, Special Publications. Forschungsinstitut und Natur-Museum Senckenberg. Senckenberg-Anlage 25, D-6000 Frankfurt am Main 1, Germany. Publication : Senckenbergiana Lethea. International Federation of Palynologicaf Societies . D.M. Jarzen, National Museum of Natural Sciences, Paleo­ biology Division, Ottawa, Ontario KIA OM8, Canada. Palaeobotanical Society. 53 University Road, Lucknow, India . Publication : Geophytology. Palaeontological Society of China. (Founded, 1929; member­ ship, 1200) Nanjing Institute of Geology and Palaeon­ tology, Chi-Ming-Ssu, Nanjing 210009, People's Republic of China . Publications : Acta Palaeontologica Sinica, Acta Micropalaeontologica Sinica. Palaeontological Society of India . 98 Mahatama Gandhi Marg, Lucknow, India. Publication: Journal of the Palae­ ontological Society of India. Palaeontological Society of Japan (Nippon Koseibutsu Gakkai) . (Founded, 1935; membership, 720) Department of Geology, Kyushu University, Fukuoka (Hakata) 812, Japan . Publications : Transactions and Proceedings, Special Papers, Fossils . Palaontologische Gesellschaft. (Founded, 1912; membership, 950) Forschungsinstitut Senckenberg, Senckenberg­ Anlage 25, D-6000 Frankfurt am Main 1, Germany . Publication : Paliiontologische Zeitschrift. Palynological Society of India . (Founded, 1965; membership, 205) 24B/5 Original Road, New Delhi 1 10005, India. Pub­ lication : Journal of Palynology. Schweizerische Palaontologische Gesellschaft. (Founded, 1921; membership, 198) Birkhaeuser Verlag, PO Box 133, CH-4010 Basel, Switzerland . Publication: Schweizerische Paliiontologische Abhandlungen . Sociedad Espafiola de Paleontologia. Enadmisa, Doctor Esquerdo 138, 28007 Madrid, Spain . Publications: Revista Espanola de Paleontologia, Revista Espanola de Micropaleon tologia. Societa Paleontologica Italiana. Instituto di Paleontologia, Via Universita n. 4, 41 100 Modena, Italy. Publication: Bollettino della Societii Paleontologica Italiana. Vsesoyuznoe Paleontologischekoe Obshchestvo . Leningrad, U.5.5.R. Publication: Trudy Sessii.

Appendix 11: Serial publications supplementary list These Serial publications are listed in the following format: name of publication; International Standard Serial Number (ISSN); first year of publication; type of publication (P, periodical; MS, monograph series); periodicity (qu, quar­ terly; bi-m, bi-monthly; irreg, irregular; ann, annual; bi-ann, bi-annual); language(s) of text and summaries; parent body (society, institute, or publisher) and address; distributor (if different from parent body) and address; current (1989) editor

6 . 4 Societies, Organizations, Journals, and Collections (ed . 1989); circulation (circ); average number of pages per year (pp/yr); size of pages (cm); indexing, abstracting, and online services; CODEN; and other publications from the same parent body.

Acta Micropalaeontologica Sinica. ISSN 1000- 0674; 1984 - ; P; qu; Chinese, summaries i n English; Palaeontological Society of China; Science Press, Beijing; distributed by China International Book Trading Corporation (Guoji Shudian), PO Box 2820, Beijing, Peoples Republic of China; 450 pp/yr; 14 x 22 cm; indexed in BioI. Abstr. , GeoRef; see also Acta Palaeontologica Sinica . Acta Palaeobotanica . ISSN 000 1 - 6594; 1960 - ; P; qu; Polish, summaries in English; Panstwowe Wydawnictwo Nankowe Oddzial, Krak6w, Poland; indexed in GeoRef; CODEN, APBCAG . Acta Palaeontologica Polonica . ISSN 0567- 7920; 1956 - ; P; qu; English, French, Polish, summaries in Polish and Russian; InstytutPaleobiologii PAN, Aleja Zwirki i Wigury93,02-D89 Warsaw, Poland; ed., J. Dzik; circ 700; 440 pp/yr; 12.6 x 1 9.6 cm; indexed in BioI. Abstr., Bull. Sig., GeoRef, Ref. Zhur., Zoo. Rec., CODEN, APGPAC. Acta Palaeontologica Sinica . ISSN 000 1 - 6616; 1953 - ; P; bi-m; Chinese, summaries in English; Palaeontological Society of China; Institute of Scientific and Technological Information of China, China Publications Centre, Chegongzhuang Xilu 21, PO Box 339, Beijing, Peoples Republic of China; 700 pp/yr; 15.5 x 22 .5 cm; indexed in BioI. Abstr., GeoRef; CODEN, KSWHAT; see also Acta Micropalaeontologica Sinica. Ameghiniana. ISSN 0002- 7014; 1957 - ; P; qu; English and Spanish, summaries in English and Portuguese; Associaci6n Paleontol6gica Argentina, Maipu 645, Primer Piso 1 - 5047, 1006 Buenos Aires, Argentina; ed, G.J. Scillato Yane; circ. 1000; indexed in BioI. Abstr., GeoRef; CODEN, AMGHB2 . Annales de Paleontologie. ISSN 0753 -3969; 1982- (Vol . 68, no. 1); P; qu; French, summaries in English; Masson et Cie, 120 bd. St. Germain, 75280 Paris Cedex 06, France; ed . , B . Badre, Laboratoire d e Paleontologie des Vertebres & PaIeontologie humaine, Universite Paris VI, 4 place Jussieu, 75230 Paris Cedex 05, France; circ 700; 350 pp/yr; 12 x 19 cm; indexed in BioI. Abstr., Bull. Sig., GeoRef, Pascal Folio. Merger of Annales de Paleontologie: Vertebres (ISSN 0570 - 1627) 1964- and Annales de Paleontologie: Invertebres (lSSN 0570- 1619) . Beitriige zur Paliiontologie von Osterreich . 1976 - ; P; irreg; German and English; O sterreichische PaHiontologische Gesells.:haft; Palaontologisches Instituts der Universitat Wien; distributed by Kommissionsverlag Universitatsstr. 7/1 1, A-lOlO Vienna, Austria; indexed in BioI. Abstr., GeoRef; CODEN, BPOEDX. Bolletino della Societa Paleontologica Italiana . ISSN 0375- 7633; 1960 - ; P; qu; Italian Council for Scientific Research, Piazzale A. Moro 7, 00185 Rome, Italy; subscription in­ formation from Soc. Paleontologica Italiana, clo Istituto di Paleontologia, Via Universita n.4, 41 100 Modena, Italy; circ 800; indexed in BioI. Abstr., GeoRef; CODEN, BSPIAY . Bulletin of the British Museum (Natural History), Geology Series. ISSN 0007- 1471 ; 1949 - ; MS; irreg; English; The

531

Natural History Museum, Cromwell Road, London SW7 5BD, U . K . ; circ 700; 300 pp/vo!; 14.4 x 21 . 5 cm (B4); indexed in BioI. Abstr., GeoRef, Zoo. Rec. ; CODEN, BUBMAO. Bulletins of American Paleontology. ISSN 0007- 5779; 1895 - ; MS; bi-ann; English. Palaeontological Research Institution, 1259 Trumansburg Rd, Ithaca, New York 14850 - 1398, U.5.A . ; ed . , P.B. Hoover; circ 500; indexed in BioI. Abstr., GeoRef; CODEN, BAPLAJ; see also Palaeontographica Americana. Cahiers de Micropaleontologie. ISSN 0068- 5054; 1965 - ; MS; irreg; French, summaries in English; Editions du CNRS, 15 Quai Anatole France, F- 75700 Paris, France; indexed in Brit. GeoI. Lit . , Geo. Abstr. , GeoRef. Communicaciones Paleontologicas : Museo Nacional de Historia Natural . 1970 - ; P; irreg; Spanish, summaries in English; Museo Nacional de Historia Natural, Casilla de Correos 399, Montevideo, Uraguay. Contributions from the Institute of Geology and Palaeon­ tology, Tohoku University. ISSN 0082-4658; 1921 - ; irreg; Japanese, summaries in English; Tohoku University, Institute of Geology and Palaeontology - Tohoku Daigaku Rigakubu Chishitsugaku Koseilbutsugaku Kyoshitsu, Aobayama, Sendai 980, Japan; circ 750, indexed in BioI. Abstr., GeoRef. Contributions from the Museum of Palaeontology: University of Michigan. ISSN 0097- 3556; 1924 - ; irreg; English; University of Michigan, Museum of Paleontology, Museums Building, Ann Arbor, MI 48109, U . 5 . A . ; ed . , G . R. Smith; circ 500; indexed i n BioI. Abstr., GeoRef; CODEN, UMMPA3; see also University of Michigan Museum of Paleontology: Papers on Palaeontology. Contributions to Canadian Palaeontology, Geological Survey of Canada, Bulletin . ISSN 0068- 7626; 1988 - ; P; irreg; English, summaries in French; Geological Survey of Canada, 601 Booth St. , Ottawa, Canada KIA OE8; ed . , L. Reynolds; 18.6 x 23. 7 cm; indexed in GeoRef; CODEN, CGSBAN. Fieldiana : Geology. ISSN 0096 -2651; 1985 - ; irreg; English; Field Museum of Natural History, Roosevelt Road at Lake Shore Drive, Chicago, IL 60605 -2496, U . 5 . A . ; ed . , T. Plowman; circ 450; indexed in BioI. Abstr., Chem. Abstr. , GeoRef· Folia Geobotanica et Phytotaxonomica. ISSN 0015-5551 ; 1966 - ; P ; qu; English, French, German, summaries in English and German; Ceskoslovenska Akademie Ved, Botanicky Ustav, Vodickova 40, 1 1229 Prague 1, Czechoslovakia; distributed by Junk, B.V., Lange, Voorhout 9 - 1 1 , The Hague, Netherlands; circ 1 100; indexed in BioI. Abstr., Geo. Abstr. , GeoRef; previously Folia Geobotanica et Phyto­ taxonomica Bohemoslavaca; CODEN, FGPHAP. Geologica Hungarica, Series Palaeontologica. ISSN 0374 - 1 893; 1928 - ; irreg; English, French, German, Hungarian, Russian. Magyar Allami Foldtani Intezet, Budapest, Hungary; distributed by Collets Holdings Ltd . , Denington Estate, Wellingborough, U . K . ; indexed in BioI. Abstr., GeoRef; CODEN, GHPADH. Geophytology. ISSN 0376- 5156; 1971 - ; P; English; Palaeo­ botanical Society, 53 University Road, Lucknow 7, India; circ 240; indexed in BioI. Abstr., GeoRef; CODEN, GPHTAR.

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6 Infrastructure of Palaeobiology

Journal of Foraminiferal Research . ISSN 0096- 1191; 1971 - ; P ; qu ; English; Cushman Foundation for Foraminiferal Research, Museum of Comparative Zoology, Invertebrate Paleontology, Harvard University, 26 Oxford Street, Cambridge, MA 021 38, US.A; ed., P. Loubere; circ 800; indexed in Bioi. Abstr., S.c.!., Br. Geol. Lit., Geo. Abstr., GeoRef; CODEN JFARAH; see also Special Publication: Cushman Foundation. Journal of Palynology. ISSN 0022 -33979; 1966- ; P; English; Palynological Society of India; distributed by Today and Tommorow's Printers, 24 B/5 Original Road, New Delhi 110005, India; ed, P.K.K. Nair; circ 400; indexed in BioI. Abstr., GeoRej. Journal of the Palaeontological Society of India. ISSN 0552 9360; 1956 - ; P; English; distributed by Indian Books and Periodicals Syndicate, B-5/62 Dev . Nagar P . O . Road, Karol Bagh, New Delhi, 1 1 0005, India; circ 1 000; indexed GeoRef; CODEN, PLSIB] . Marine Micropaleontology. ISSN 0377-8398; 1976 - ; P; qu; English; Elsevier Science Publishers, PO Box 21 1, 1000 AE Amsterdam, The Netherlands; indexed in BioI. Abstr. , Curr. Cont., Geo. Abstr. , GeoRef, Mar. Sci. Cont. Tab. , S . C . I. ; CODEN, MAMIDH. Memoir (Paleontological Society) . ISSN 0022- 3360; 1968 - ; MS; irreg; English; see under Paleontological Society; ed. D . C Steinker, Dept . Geology, Bowling Green State University, Bowling Green OH 43403, U S A . ; circ 3000; 74 pp/ issue; 21 .5 X 28 cm; indexed in BioI. Abstr. , GeoRef; CODEN, PSMECR; see also Journal of Paleontology and Paleobiology . Memoir of the Association of Australasian Palaeontologists . ISSN 0810- 8889; 1983 - ; irreg; English; Geological Society of Australia, 606 AN.A House, 301 George Street, Sydney, New South Wales 2000, Australia; see also Alcheringa. Memoirs of the Institute of Vertebrate Paleontology and Paleo­ anthropology. Academia Sinica, Institute of Vertebrate Palaeontology and Palaeoanthropology, Beijing 28, Peoples Republic of China; CODEN, CKKKD7; see also Palaeon­ tologia Sinica and Vertebrata Palasiatica. Michigan State University: Museum Publications, Paleon­ tological Series . 1972 - ; irreg; English; Michigan State University Museum, East Lansing, MI 48824, U . 5 . A ; circ 1500. Neues Jahrbuch fUr Geologie und Paliiontologie, Abhandlungen . ISSN 0077- 7749; 1870 - ; irreg (3 nos/vo!, 2-3 vols/yr); German and English; E. Schweizerbart'sche Verlagsbuch­ handlung, Johannesstr. 3A, D-7000 Stuttgart 1, Germany; circ 650; 15.5 x 23 . 3 cm; indexed in BioI. Abstr. , Chem . Abstr., GeoRef, Petrol. Abstr. ; CODEN, NEJPAP; see also Monatshefte below . Neues Jahrbuch fUr Geologie und Paliiontologie, Monatshefte. ISSN 0028 - 3630; 1900 - ; monthly; German and English; E. Schweizerbart'sche Verlagsbuchhandlung, Johannesstr. 3A, D-7000 Stuttgart 1, Germany; circ 768; 14.7 x 22 cm; indexed in BioI . Abstr. , Chem . Abstr., GeoRef, Petrol. Abstr. ; CODEN, NJGMA2; see also Abhandlungen above. New South Wales Geological Survey Memoirs : Palaeontology. ISSN 0077- 8699; 1888 - ; MS; irreg; English; Dept. of Mineral Resources, Box 5288, Sydney, New South Wales 2001, Australia; ed, H. Basden; circ 400; indexed in GeoRej.

New Zealand Geological Survey: Palaeontological Bulletin . ISSN 0078- 8589; 1913 - ; MS; irreg; English; D . 5 . L R. Science Information Publishing Centre, PO Box 9741, Wellington, New Zealand; ed., L Mackenzie; circ 800; indexed in BioI. Abstr. , Geo. Abstr., GeoRej. , Petrol. Abstr. ; CODEN, PBZGAB . Palaeobotanist. ISSN 0031 -0174; 1952 - ; 3/yr; English; Birbal Sahni Institute of Palaeobotany, 53 University Road, Lucknow 7, India; ed . , M.N. Bose; circ 400; indexed in BioI. Abstr. , GeoRef, Indian Sci. Abstr. ; CODEN, PLBOA] . Palaeogeography, Palaeoclimatology, Palaeoecology. ISSN 0031 - 0182; 1965 - ; P; 4 parts/vo! 5 vols/yr; English, French ' and German; Elsevier Science Publishers, PO Box 211, 1000 AE Amsterdam, The Netherlands; eds, P. de Deckker, C Newton & F. Surlyk; circ 1400; 19 x 26 cm; indexed in BioI. Abstr., Brit. Geol. Lit., Bull. Signal., Chem. Abstr., Curr. Cont., Geo. Abstr., GeoRef, Ocean Abstr., Pascal Folio, Petrol. Abstr., S.c.!.; CODEN PPPYAB. Palaeontographica Americana. ISSN 0078 - 8546; 191 6 - ; MS; irreg; English; Paleontological Research Institute, 1259 Trumansburg Road, Ithaca, New York 14850, U . 5 . A . ; ed . , P . R . Hoover; circ 400; 21 . 8 x 2 8 cm; indexed i n BioI. Abstr. , Geo. Abstr. , GeoRef; CODEN, PALAAI; see also Bulletins of American Paleontology. Palaeontographica Canadiana . ISSN 0821 - 7556; 1983 - ; MS; irreg; Joint Committee on Paleontological Monographs of the Canadian Society of Petroleum Geologists and the Geological Association of Canada, Dept . of Earth Sciences, Memorial University, St. John's, Newfoundland AIB 3X5, Canada; ed., R. Ludvigsen; circ 600; 1 15 pp/no; 21 . 5 x 28 cm; indexed in GeoRef. Palaeontologia Africana. ISSN 0078 - 8554; 1953 - ; P; irreg; English; Bernard Price Institute for Palaeontological Research, University of the Witwatersrand, 1 Jan Smuts Avenue, Johannesburg 2001, South Africa; ed . , M.A. Raath; circ 600; 17.5 x 24. 5 cm; indexed in BioI . Abstr., GeoRef; CODEN, PBPRAS. Palaeontologia Jugoslavica. ISSN 0552 -9352; 1958 - ; P; qu; Serbo-Croatian, English, French, German; Jugoslavenska Akademija Znanosti i Umjetnosti, Brace Kavurica 1, 41000 Zagreb, Yugoslavia; ed., Malaz; indexed in BioI. Abstr. , GeoRej., Zent. Math . ; CODEN, PLJUA9 . Palaeontologia Polonica. ISSN 0078 -8562; 1929 - ; MS; irreg; English, summaries in Polish; Polish Academy of Sciences, Institute of Paleobiology, AI . Zwirki i Wigury 93, 02 - 098 Warszawa, Poland; distributed by Ars Polona­ Ruch, Krakowskie Przedmiescie 7, 00-068 Warszawa, Poland; 15.4 x 23 .6 cm; indexed in BioI. Abstr. , GeoRef; CODEN, PLPOAL Palaeovertebrata . ISSN 0031 - 0247; 1967- ; P; qu; French, English, German, Spanish; Laboratoire de Paleontologie, Place Eugene Bataillon, 34060 Montpellier Cedex, France; ed., B. Sige; circ 200; indexed in Bull. Signal. , GeoRef; CODEN, PLVTAW. Palaios . ISSN 0883- 1351 ; 1986 - ; P; bi-m; English; Society of Economic Paleontologists and Mineralogists, PO Box 4756, Tulsa, OK 74159 -0756, U S A . ; ed . , D.]. Bottjer; circ 2000; 17.6 x 25 .2 cm; 600 pp/yr; indexed in GeoRej. Paleobiologie Continentale. ISSN 0750- 7488; 1970 - ; Universite des Sciences e t Techniques, Laboratoire de

6 . 4 Societies, Organizations, Journals, and Collections Paleobotanique, Montpellier, France; CODEN, PACOD1. Paleobios . ISSN 0031 - 0298; 1967 - ; MS; irreg; English; Museum of Paleontology, University of California, Berkeley, CA 97420, U . S . A . ; ed . , M . G . Kellog; circ 1000; indexed in GeoRef. CODEN, PLB1AZ . Paleontologia y Evoluci6n . ISSN 021 1 - 609X; 1979 - ; Spanish; Instituto de Paleontologia, Barcelona, Spain. Paleontologia Mexicana. ISSN 0185-478X; 1954- ; MS; irreg; Spanish; Universidad Nacional Aut6noma de Mexico, Instituto de Geologia, Ciudad Universitaria, 04510 Mexico; indexed in GeoRef; CODEN, MUGPA9 . Paleontologicheskiy Sbornik (L'vov) . ISSN 0131 - 2634; 1961 - ; Russian; Izdatel'stvo L'vovskogo Universiteta, U . 5 . 5 . R . ; indexed i n GeoRef; CODEN, PALSA4. Quartiirpaliiontologie. ISSN 0138 - 3116; 1975 - ; irreg; English, French, German, Russian; Institut fur Quartarpalaon­ tologie, Akademie-Verlag Berlin, Leipziger Str. 3 - 4, 1086 Berlin, Germany; ed., H . D . Kahlke; indexed in GeoRef; CODEN, QUARDW. Revista Espaiiola de Paleontologia. 1986 - ; P; Spanish and English; Sociedad Espafiola de Paleontologia, Museo Nacional de Ciencias Naturales, clJose Gutierrez Abascal 2, 28006 Madrid, Spain; circ 100; A4; see also Revista Espaiiola de Micropaleontologia below. Revista Espaiiola de Micropaleontologia. ISSN 0556 - 655X; 1969 - ; P; 3/yr; Spanish; Enadmisa, Doctor Esquerdo 138, 28007 Madrid, Spain; circ 700; indexed in BioI. Abstr., GeoRef; CODEN, RTEMB5; see also Revista Espaiiola de Paleontologia above. Revue de Micropaleontologie. ISSN 0035- 1 598; 1958 - ; P; qu; French and English; Maison de la Geologie, BP 1 1 - 705, 75224 Paris Cedex 05, France; ed, M. Neumann; circ 700; 270 pp/vol; 21 x 27 cm; indexed in Brit. Geol. Lit., GeoRef, Pascal Folio, Petrol. Abstr. ; CODEN, RTEMB5 . Revue de Paleobiologie. ISSN 0253- 6730; 1982 - ; P; French and English; Museum d'Histoire Naturelle de Geneve, 1 Route de Malagnou, CP 434, 121 1 Geneva 6, Switzerland . Rivista Italiana d i Paleontologia e StratigraJia. ISSN 0035 - 6883; 1895 - ; P; qu; Italian, English, French, and German; Dipartimento di Scienze Terra, Universita Milano, Via Mangiagalli 34, Milan, Italy; circ 450; indexed in BioI. Abstr. , Geo. Abstr., GeoRef, Petrol. Abstr. ; CODEN, RPLSAT. Also Memoria ISSN 0375- 9784; MS; Italian, summaries in English; CODEN, RVPMA5 . Sbornik Geologickydi Ved. Paleontogie ( Journal of Geological Sciences, Palaeontology) . ISSN 0036- 5297; 1949 - ; irreg; Czech, English, German, and summaries in Czech and Russian; Ustredni Ustav Geologicky, Malostranske nam . 19, 1 1 8 21 Prague 1, Czechoslovakia; distributed by Artia, PO 790 VE Smeckach, Prague 1, Czechoslovakia; circ 600; indexed in Bull. Sig., GeoRef, Ref. Zhur. ; CODEN,SGPABC. Schweizerische Palaeontologische Abhandlungen . ISSN 00807389; 1 874 - ; MS; irreg; German, French, English, and Italian; Schweizerische Palaontologische Gesellschaft; dis­ tributed by Birkhaeuser Verlag, PO Box 133, CH-4010 Basel, Switzerland; ed, B . Engesser; indexed in BioI . Abstr. , GeoRef; CODEN, SPAAAX. Senckenbergiana Lethaea . ISSN 0037-2110; 1919 - ; P; 6/yr; German, French, and English; Senckenbergische Naturforschende Gesellschaft, Senckenberganlage 25, D=

533

6000 Frankfurt 1, Germany; distributed by Verlag Dr Waldemar Kramer, Bornheimer Landwher 57A, D-6000 Frankfurt 60; ed., H. Malz; circ 850; indexed in BioI. Abstr. , Brit. Geol. Lit., Chem . Abstr. , GeoRef; CODEN, SLETAE . Smithsonian Contributions to Paleobiology. ISSN 008 1 - 0266; 1969 - ; MS; irreg; English; Smithsonian Institute Press, PO Box 1579, Washington, DC 20013, U . 5 . A . ; circ 3000; 21 . 5 x 28 cm; indexed in BioI. Abstr. , GeoRef; CODEN, SPBYA8 . Special Papers - Palaeontological Society of Japan . ISSN 0549 3927; CODEN, SPPAB7; see also Transactions and Proceed­ ings of the Palaeontological Society of Japan below. Special Papers in Palaeontology. ISSN 0038- 6804; 1967 - ; 2Iyr; English, Palaeontological Association (see above); distrib­ uted by Marston Book Services, Osney Mead, Oxford OX 2 OEL, U.K. ; circ 300; c. 160 pp/no; 19 x 24. 5 cm; indexed in BioI. Abstr. , GeoRef. CODEN, SPPAB7. Special Publication : Cushman Foundation for Foraminiferal Research. ISSN 0070- 2242; 1952 - ; irreg; English; Cushman Foundation for Foraminiferal Research. Museum of Comparative Zoology, Invertebrate Paleontology, Harvard University, 26 Oxford Street, Cambridge, MA 02138, U .5.A. ed., S.J. Culver; circ 600; indexed in Bioi. Abstr., GeoRef; CODEN, SPCFAO; see also Journal of Foraminiferal Research. Stereo-Atlas of Ostracod Shells. ISSN 0952 - 745 1 ; 1973 - ; bi­ ann; English; British Micropalaeontological Society; ed . , D . J . Siveter, Department o f Geology, The University, Leicester LE1 7RH, U . K . ; circ 400; 1 60 pp/yr; 23. 8 x 30. 8 cm; indexed in GeoRef. Transactions and Proceedings of the Palaeontological Society of Japan . ISSN 0031 - 0204; 1935 - ; P; qu; English, summaries in Japanese; Palaeontological Society of Japan (Nihon Koseibutsu Gakkai), clo Japan Academic Societies Centre, 2-4-16 Yayoi, Bunkyo-ku, Tokyo 1 13, Japan; eds, 1 . Hayami & I . Obata; circ 550; indexed i n BioI. Abstr., GeoRef., Petrol. Abstr. ; CODEN, TPPJAA. Trudy Paleontologicheskogo Instituta. ISSN 0376- 1444; 1932 - ; P ; Russian; Akademiya Nauk SSSR, Paleontologicheskiy Institut, Profsoyuznayas 113, S-1 1 7321 Moscow, U . 5 . 5 . R . ; indexed i n GeoRef; CODEN, TPIAAG . Tulane Studies in Geology and Palaeontology. ISSN 0041 -4018; 1962 - ; qu; English; Tulane University, Department of Geology, New Orleans, LA 701 1 8, U . 5 . A . ; eds, H . C . Skinner & E . H . Yokes; circ 1000; indexed i n Chem . Abstr., GeoRef, Petrol. Abstr. ; CODEN, TSGEB6. University of Kansas Paleontological Contributions: Articles. ISSN 0075 - 5044; 1947 - ; MS; irreg; English; CODEN, KUPABM. Monographs ISSN 0278-9744; 1982 - ; MS; irreg; English . Papers ISSN 0075 -5052; 1965 - ; MS; irreg; English; CODEN,KCPA3. University of Kansas, Paleon­ tological Institute, 121 Lindley Hall, Lawrence, KS 66045, U.S.A. ; ed . , R.L. Kaesler; circ 1500; indexed in BioI. Abstr., Geo. Abstr. , GeoRef. University of Michigan Museum of Paleontology: Contributions . ISSN 0041 - 9834; 1924 - ; irreg; English. Papers on Paleontology. ISSN 0148- 3838; MS; irreg; English; CODEN, PPUMD3 . University of Michigan, Museum of Paleontology, Ann Arbor, MI 48109, U.5 .A; circ 500;

534

6

Infrastructure of Palaeobiology

indexed in BioI. Abstr. , GeoRef. Utrecht Micropaleontological Bulletins . ISSN 0083-4963; 1969 - ; MS; irreg; English; CODEN, UfMBAA. Special Publications . ISSN 0165 - 2753; MS; irreg; English; CODEN, UMBPD] . Rijksuniversiteit tu Utrecht, Dept. of Stratigraphy and Paleontology, do T. van Schaik, Budapestlaan 4, 3584 CD Utrecht, The Netherlands; indexed in GeoRef. Vertebrata Palasiatica. ISSN 0042 -4404; Academia Sinica, Laboratory of Vertebrate Paleontology, Beijing, China; indexed in GeoRef., S . C . I. ; CODEN, VEPAAU; see also Memoirs of the Institute of Vertebrate Paleontology and Paleoanthropology and Palaeontologica Sinica. Voprosy Mikropaleontologii. ISSN 0507- 3693; 1956 - ; Russian; Akademiya Nauk Ordena Trudovogo Krasnogo Znameni Geologicheskiy Institut, Moscow, U . 5 . 5 . R . ; indexed in GeoRef; CODEN, VMlKAD. Voprosy Stratigraffi i Paleontologii. ISSN 0134 - 8698; 1975 - ; Russian; Izdatelstvo Saratevskogo Universiteta, Saratov, U.S.S.R.

Appendix Ill: Bibliographical publications For an explanation of abbreviations, please see Appendix 11.

Bibliographie Palynologie. ISSN 0766- 5679; 1975- (supple­ ment to Pollen et Spores); French; eds, M. Van Campo, M. and C. Millerand, Laboratoire de Palynologie, Universite des Sciences et Techniques du Languedoc, 34060 Montpellier Cedex, France; indexed in GeoRef. Bibliography and Index of Geology. ISSN 0098- 2784; 1969 - ; monthly; English; ed . , G . N . Rassam, American Geological Institute, 4220 King St. , Alexandria, VA 22302 - 1507, U . S . A . ; circ 900; available online, CISTI, DIALOG, Orbit Information Technologies. Formed by merger of Bibliography of North American Geology and Bibliography and Index of Geology Exclusive of North America . Bibliography and Index of Micropaleontology. ISSN 0300- 7227; 1972 - ; monthly; English; ed . , S. Carroll, Micropaleon­ tology Press, do American Museum of Natural History, Central Park West at 79 St. , New York, NY 1 0024, U . 5 . A . ; circ 250; available online, CISTI . Bibliography of Fossil Vertebrates. ISSN 0272- 8869; 1940 - ; ann; English; Society o f Vertebrate Paleontology, do Natural History Museum of Los Angeles County, 900 Exposition Blvd . , Los Angeles, CA 90007, U . 5 . A . ; indexed in GeoRef. Bibliography of North American Paleobotany. Botanical Society of America, Paleobotanical Section; ed . , G.W. Rothwell, Dept . Botany, Ohio University, Athens, OH 45701, U.5.A. Biological Abstracts . ISSN 0006-3169; 1927 - ; monthly; English; BioSciences Information Service (810SIS), 2100 Arch Street, Philadelphia, PA 19103 - 1399, U . 5 . A . ; avail­ able online, BRS, CISTI, Central Institute for Scientific and Technical Information, DIMDI, Data-Star, DIALOG, European Space Agency, ]ICST, Mead Data General, STN International; indexed in Anim. Breed. Abstr., Ind. Vet. , JAMA, Popul. Ind., Rev. Plant Path . , VITIS, Vet. Bull. British Geological Literature. ISSN 0140 - 7813; 1972 - ; qu; English; ed . N . Edwards, Bibliographic Press Ltd . , 52

Little Paddocks, Ferring, Worthing, West Sussex BN12 5NH, U . K . ; circ 300. Bulletin SignaIetique. Bibliographie des Sciences de la Terre 227: Paleontologie. ISSN 0300 -9335; 1972 - 84; French; Editions du CNRS, 23 rue du Maroc, 75019 Paris, France; see Pascal Folio. Catalog of Fossil Spores and Pollen. ISSN 0148- 642X; 1957 - ; 3/yr; English; e d . , W . Spackman, Pennsylvania State University, Coal Research Station, Deike 517, College of Earth and Mineral Sciences, University Park, PA 16802, U.5.A . ; circ 600 . Catalogue of Conodonts. Irreg; English; ed . , W. Ziegler, E. Schweizerbartsche Verlag, ]ohannesstr. 3-A, D-7000 Stuttgart 1, Germany . Current Contents/Life Science. ISSN 001 1 - 3409; 1958- ; English; Institute for Scientific Information, 3501 Market St. , Philadelphia, PA 19104, U . 5 . A . ; and 132 High St., Uxbridge, Middlesex UB8 1DP, U.K. ; available online, BRS; indexed in Abstr. Bull. Inst. Pap. Chem. , Abstr. Hyg. Compumath, Ind. Sci. Rev., SSCI, Sri. Cit. Ind. Ellis and Messina Catalogues of Micropaleontology. English; ed . , S . E . Carroll, Micropaleontology Press, do American Museum of Natural History, Central Park West at 79th St. , New York, NY 10024, U . 5 . A . ; including Catalogue of Diatoms, Catalogue of Foraminifera, Catalogue of Ostracoda . Geological Abstracts : Palaeontology and Stratigraphy. ISSN 0268- 8018; 1986 - ; bi-m; English; ed., A. Cruikshank, Geo Abstracts Ltd . , Regency House, 34 Duke St. , Norwich NR3 3AP, U . K . ; circ 300. Geotitles . 1969 - ; English; monthly; Geosystems, PO Box 40, Didcot, Oxfordshire OX1 1 9BX, U.K. ; available online, DIALOG; formerly Geotitles Weekly. Pascal Folio. Part 47: Paleontologie. 1985 - ; 10/yr; French (Bureau de Recherches Geologiques et Minieres); Centre National de la Recherche Scientifique, Centre de Documentation Scientifique et Technique, Service des Abonnements, 26 rue Boyer, 75971 Paris 20, France; supersedes Bulletin Signaletique. Referativnyi Zhurnal . ISSN 0486 -2309; 1954 - ; monthly; Russian; Vsesoyoznyi Institut Nauchno-Technicheskoi Informatsii (VINITI), Baltiiskaya ul . 14, Moscow A-219, U . S . 5 . R . ; subscription information for Mezhdunarodnaya Kniga, Dimitrova ul. 39, 113095, Moscow, U.5.5.R.; indexed in Chem . Abstr. Zentralblatt fii r Geologie und Palaeontologie. Teil II. Palaeon­ tologie. ISSN 0044 -4189; 1807 - ; 7/yr; German; eds, A. and E. Seilacher, E. Schweizerbart'sche Verlagsbuchhandlung, ]ohannesstr. 3A, D-7000 Stuttgart 1, Germany; indexed, Chem . Abstr. Zoological Record. ISSN 0084- 5604; 1864 - ; English; eds, H . G . Vevers & M.A. Edwards (Zoological Society o f London), BioSciences Information Service (810SIS) U.K., Garforth House, 54 Micklegate, Boston Spa, Yorkshire Y01 1LF, U.K. ; indexed, Helminthol. Abstr. ; available online, BRS, DIALOG .

6 . 4 Societies, Organizations, Journals, and Collections

535

Appendix IV: Museums housing major fossil collections

Spain Madrid : Museo Nacional de Ciencias Naturales, Paseo de la Castellana 84, Madrid 6

Europe

Sweden Lunds: Lunds Universitet, Palaeontologiska Institutionen, Fack, 221 01 Lund 1 Stockholm: Naturhistoriska Riksmuseet, Stockholm 50 Uppsala : Zoologiska Museum, Palaeontological Institut, Universitet i Uppsala

Austria Vienna: Naturhistorisches Museum, Wien, Burgring 7, A1014, Vienna Belgium Brussels: Institut Royale des Sciences Naturelles de Belgique, 31 Rue Vautier, B-1040 Brussels Czechoslovakia Prague: Narodni Muzeum, Vaclavske namesti, 1 700, Prague 1 Denmark Copenhagen: Dansk Geologisk Forening, Mineralogisk Museum, 7 0ster Voldgade, 1350 Copenhagen K France Lyons: Universite de Lyon I, Department des Sciences de la Terre, 43 Boulevard du 11 Novembre, 69622 Villeurbanne Cedex Paris : Museum National d'Histoire Naturelle, Jardin des Plantes, 57 Rue Cuvier, 75281 Paris Cedex 05 Germany Berlin : Humboldt Universitat, Museum fUr Naturkunde, Palaontologisches Museum, Invalidenstrasse 43, 104 Berlin Frankfurt am Main: Senckenberg Naturmuseum, 25 Senckenbergan-Anlage, D-6000, Frankfurt am Main 1 (Publication: Senckenbergiana Lethaea) Munich: Bayerische Staatssammlung fUr Palaontologie und Historische Geologie, Richard Wagner-Strasse 10, D-800 Miinchen 2 Ireland, Republic of Dublin: National Museum, Geology Department, Merrion Row, Dublin 2 Italy Florence : Museo di Paleontologia dell'Universita di Firenze Milan: Museo Civico di Storia Naturale di Milano, Corso Venezia 55, 1-20121 Milano Verona: Museo Civico di Storia Naturale di Verona, Lungadige Porta Vittoria 9, 1 - 37100 Verona Netherlands Haarlem: Teylers Museum, Damstraat 21, Haarlem Leyden: Riijksmuseum van Geologie en Mineralogie, Hooglandse Kerkgracht 17, NL-2312 HS, Leyden Norway Oslo : Universitets Paleontologiska Museum, Sars Gate 1, Oslo 5 Poland Warsaw: Muzeum Ziemi PAN, Polish Academy of Sciences, Palaeozoological Division, Al. Na Skarpie 20-26, PL-OO488, Warszawa

Swi tzerland Basel : Naturhistorisches Museum, Augustinergasse, 2, CH4000 Basle Geneva: Museum d'Histoire Naturelle, route de Malagnou, 1211 Geneva 6 (Publication : Revue de Paleobiologie) Lausanne : Musee Geologique, Palais de Rumine, 1005 Lausanne United Kingdom Birmingham: University Museum, Department of Geological Sciences, PO Box 363, Birmingham B15 2TT Cambridge : Sedgwick Museum, Downing Street, Cambridge CB2 3EQ Keyworth: British Geological Survey, Keyworth NG12 5GG London : British Museum (Natural History), Cromwell Road, London SW7 5BI . (Publication : Bulletin of the British Museum (Natural History), Geology Series) Manchester: Manchester Museum, The University, Oxford Road, Manchester M13 9PL Oxford: University Museum, Parks Road, Oxford OXl 3PW Edinburgh: Royal Scottish Museum, Chambers Street, Edinburgh EHl 1JF Edinburgh: British Geological Survey, Murchison House, West Mains Road, Edinburgh EH9 3LA Glasgow: Hunterian Museum, Glasgow University, Depart­ ment of Geology, Glasgow G12 8QQ Cardiff: National Museum of Wales, Cathays Park, Cardiff CF1 3NP Belfast: The Ulster Museum, Botanic Gardens, Belfast BT9 5AB U. S . S.R. Leningrad : Vsesoyuznyi Nauchno-Isledovatel'skij Geologi­ cheskij institut (VSEGEI), Srednij prospekt 74, SU 199026, Leningrad Kiev: Scientific Nature Research Museum, Academy of Sciences, Ukraine RSR Moscow : Palaeontological Institute, Academy of Sciences, Profsoyuzhayes 1 13, S-1 17321 Moscow (Publication: Trudy Paleontologicheskogo Instituta) Novosibirisk: Institute of Geology and Geophysics, Siberian Branch of the Academy of Sciences, SU-630090 Novosi­ birsk

North America Canada Drumheller, Alberta: Tyrrell Museum of Palaeontology, P . O . Box 7500, Alberta TOJ OYO

536

6

Infrastructure of Palaeobiology

Ottawa: National Museum of Canada 1767, Geological Survey of Canada, 601 Booth Street, Ottawa, Ontario K1A OE8 Toronto: Royal Ontario Museum, 100 Queen's Park, Toronto, Ontario M5S 2C6

Melbourne: National Museum of Victoria, 285 - 321 Russell Street, Melbourne, Victoria 3000 Sydney: Australian Museum, 6 - 8 College Street, Sydney, New South Wales 2000

U. 5.A. Ann Arbor: Museum of Paleontology, University of Michi­ gan, Ann Arbor, MI 48109 (Publications : Contributions; Papers on Paleontology) Cambridge : Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138 Chicago : Field Museum of Natural History, Roosevelt Road and Lake Shore Drive, Chicago 5, IL 60605 (Publication: Fieldiana: Geology) East Lansing: Michigan State University Museum, East Lansing, MI 48824 (Publication : Museum Publications Paleontological Series) Los Angeles : County Museum of Natural History, Exposition Boulevard, Los Angeles, CA 90007 Newhaven: Peabody Museum, Yale University, New Haven, CT 06520 New York: American Museum of Natural History, Central Park West at 79th Street, New York, NY 10024 (Publication : Micropaleontology) Pittsburgh: Carnegie Museum of Natural History, 440 New York Forbes Avenue, Pittsburgh, PA Washington: Smithsonian Institution, U . 5 . National Museum of Natural History, Washington DC 20560 (Publication : Smithsonian Contributions to Paleobiology) Utah: University of Utah, Salt Lake City, UT 84112 U . S . Geological Survey: E-501 National Museum of Natural History, Washington DC 20560

New Zealand Lower Hutt: D.5.I.R. New Zealand Geological Survey, PO Box 30 368, Lower Hutt

South America Argentina Buenos Aires : Museo Nacional Historia Naturales, Avenida Angel, Gallardo 470, Casilla de Correo 220, 1 0-Suc 5, 1405 Buenos Aires La Plata : Museo de La Plata, Paseo del Bosque 1900, La Plata Brazil Rio de Janiero: Museu Nacional, Quinta da Boa Vista, 20942 Rio de Janiero Chile Santiago : Museo Nacional de Historia Natural, Cosilla 787, Santiago Uruguay Montevideo: Museo Nacional de Historia Natural, Casilla de Correos 399, Montevideo (Publication : Communicaciones Paleon tologicas)

Australasia Australia Brisbane : Queensland Museum, Gregory Terrace, Fortitude Valley, Brisbane, Queensland 4066 Canberra: Bureau of Mineral Resources, PO Box 378, Canberra City, ACT 2601

Africa Kenya Nairobi: Institute for African Prehistory, National Museum, PO Box 40658, Nairobi South Africa, Republic of Cape Town: South African Museum, PO Box 61, Cape Town

Asia China, Peoples Republic of Beijing: Natural History Museum, 126 Tien Chiao Street, Beijing 2 Beijing: Institute of Vertebrate Paleontology and Paleo­ anthropology, Academia Sinica, PO Box 643, Beijing 28 (Publications : Memoirs) Beijing: The Geological Museum, Ministry of Geology, Xisi, Beijing Nanjing: Institute of Geology and Paleontology, Academia Sinica, 39 East Beijing Street, Chi-Ming-Ssu, Nanjing 210008, Jiangsu India Calcutta: Geological Survey of India, 27 Jawaharlal Nehru Road, Calcutta 700 016 Israel Jerusalem: Department of Geology, Institute of Earth Sciences, Hebrew University, Jerusalem 91904 Japan Tokyo: University Museum, University of Tokyo, 7-3-1 Hongo, Tokyo 1 1 3 Tokyo : Department o f Palaeontology, National Science Museum, 3-23-1 Hyakunin-cho, Shinjuku-ku, Tokyo 1 84 Sri Lanka Colombo : Colombo National Museum, P. O. Box 854 Sir Marcus Fernando Mawatha, Wanbo 7 Taiwan Taipei: Department of Geology, Taiwan Museum, 2 Siang Yang Road, Taipei

6 . 5 History of Palaeontology

6 . 5 . 1 Before Darwin

organic fossils from the inorganic. He was trying to explain the 'stoniness' that was the common feature of all his objects, and to explain the wide range of resemblances that he observed. It is difficult for a twentieth century palaeontologist to look at geologi­ cal objects with fresh eyes, and appreciate what a hard task this was (Rudwick 1972, Ch . 1 ) . Italy was the centre o f interest i n fossils i n the late sixteenth and early seventeenth centuries . Ulisse

J . C . THACKRAY

Sixteenth century beginnings

Geological objects have attracted attention since early times by their striking colours, textures, and shapes . They have been treasured as curiosities and for their medicinal or magic powers . In classical and medieval surveys such objects were described in alphabetical order, and stories recounted of their powers and virtues . With the rennaissance of the sixteenth century came a change in approach . Georgius Agricola (1494 - 1 555), a physician and apothecary in the mining town of Chemnitz in Saxony, surveyed the whole range of such objects fossils as he called them all - in De Natura Fossilium (1546) . He devised a classification, based on physical properties such as hardness, ability to take a polish, and lustre, which was a considerable advance on the earlier arrangements. Agricola believed that fossils were formed by a concreting fluid which circulated within the Earth . Twenty years later, the Swiss physician Conrad Gesner (151 6 - 1565) published De Rerum Fossilium Lapidum et Gemmarum (1565) . This was the first book on fossils to be illustrated (Fig. 1 ) . The large number of woodcuts allowed much more secure identification of the objects described than even Agricola's careful descriptions . It is also significant that Gesner based his descriptions on objects in his own collection and those of his friends . This was the start of the long connection between private and institutional collections and research . Gesner divided his geological objects into 15 classes, based on their form or material. He recog­ nized classes containing objects like plants or herbs, like parts of animals, like things in the sea, and like geometrical forms . His descriptions include the opinions of previous authors, the meaning and origin of the name, an account of the medicinal properties and the powers and virtues of the stone, and in some cases an opinion as to its origin. Gesner was not particularly concerned to separate

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537

538

6 Infrastructure of Palaeobiology

Aldrovandi (1522 - 1 605) in Bologna, Francesco Calceolari (c. 1521 -c. 1606) in Verona, and Ferrante Imperato (1550 - 1625) in Naples all built up large collections of natural and manufactured objects which included large numbers of geological speci­ mens . All three published large and well-illustrated catalogues of their collections (Torrens 1985) . A fourth collection was housed in the Vatican in Rome . Michele Mercati, who was Curator in the fifteen-sixties, prepared a catalogue which, although plates were engraved, was not published until the eighteenth century. Mercati, like Aldrovandi and others, believed that the stones in his collection, whether they were shaped like flying birds, shells, leaves, or bones, had grown within the rock by some animative or vegetative spirit . One of the plates from Mercati's unpublished catalogue was used nearly 100 years later by the Danish physician Niels Stensen (1638 - 1 686) to illus­ trate the first detailed demonstration that a particu­ lar stone could indeed be organic in origin (Fig. 2) . Stensen dissected the head of a giant shark in Florence in 1666 . He was already familiar with the fossils called 'tongue stones' found in large numbers in Malta, and their resemblance to the teeth of his shark convinced him that they were indeed part of an ancient shark. His short published account of these teeth (1667) was very different from the writings of 100 years earlier. Stensen paid no atten­ tion to the magical powers or virtues of the fossils, and was not concerned with previous opinions on their origin. He listed a series of facts, and then the conjectures based on these facts, almost like a math­ ematical theorem . His conclusion was not dogmatic; he merely indicated the lack of proof that the objects are not organic in origin (Scherz 1958) . Seventeenth century England

Stensen's work on the shark's teeth, and his later book on fossils in general, were translated into English by Henry Oldenburg, Secretary of the Royal Society . The Society, led by its Curator Robert Hooke, was the centre of a debate on the origin of fossils which lasted for 50 years from 1660 . Dis­ cussion was focused much more clearly than it had been a century before onto the problem of whether the petrified bones, shells, and teeth found in the rocks were organic remains or not. The two tech­ niques brought to bear on the problem were : study of the Bible and other sacred writings; and obser­ vations on the fossils themselves and their position in the Earth (Porter 1977; Ch . 2) .

TA B U LA I.

Fig. 2 The head of a dissected shark, engraved for Michele Mercati and published by Niels Stensen in Elementorum Myologiae Specimen (1667) .

Robert Hooke (1635 - 1703) took up one side of the debate in his lectures to the Royal Society. He maintained that it was inconceivable that fossil shells could have been formed for no purpose . As the purpose of a shell is to protect a mullusc, and the purpose of a tooth is to bite, it followed that fossil shells, bones, and teeth must be the remains of ancient animals. He realized that a few of these animals, such as ammonites, appeared to be extinct, and that the stoniness of the fossils could be ex­ plained by percolating waters . The position of fossils on inland hills and mountains he explained by the action of earthquakes, raising and lowering the land . Martin Lister (c. 1638 - 1712), a London physician, took the opposite view . He had published a book on living molluscs, and so appreciated much more clearly than Hooke that most fossils from Britain did not exactly resemble living animals . He could not accept the extinction of an animal species, and

6.5

History of Palaeontology

therefore rejected the organic origin of fossils . Two other observations confirmed his belief. He saw that many of the objects were just impressions, showing no sign of any shell, and that particular rock types appeared to have produced particular shells . Another great naturalist, John Ray (1627 - 1 705), was much less decided. He could see the arguments on both sides . On the one hand, it seemed incredible that the detailed similarities between living and fos­ sil shells, even extending to microscopic structure, should be merely fortuitous . On the other hand, the extinction of, e . g . the ammonites, suggested an im­ perfection in God's original Creation which was also incredible . Ray did suggest that perhaps fos­ sil species might not be extinct, but living in un­ explored oceans, but this did not totally satisfy him . The other problem was to account for the position of the fossils . It was generally accepted that the Flood was the only event which had affected the surface of the Earth since its formation six thousand years before, but Ray knew that fossils were not strewn over the land surface, but were embedded in rock layers . A flood deep enough to submerge the Alps was hard to explain rationally (Raven 1942, Ch . 16) . One of the great collectors of the day, John Woodward (1665 - 1728), had no doubts . He pub­ lished an Essay towards a Natural History of the Earth (1695) which confidently disposed of all these objec­ tions . He announced that fossil shells and bones were the remains of antediluvial animals that, together with the materials of the Earth's surface, had been churned up by the Flood, settling out into layers in order of their specific gravities . He accepted Ray's suggestion that unfamiliar forms would one day be found alive .

539

being considered inorganic, and in Homo Diluvii Testis (1726) the remains of a very rare antediluvian human were described . The title page of his great book on fossil plants, Herbarium Diluvianum (1709), shows Noah's Ark floating on the receding waters as shells and debris are thrown up on the shore in the foreground to become today's fossils (Jahn in Schneer 1969) . By the middle of the century there was widespread agreement that 'extraneous fossils', as petrified bones and shells had become called, were indeed the remains of ancient animals and plants . Many of the objects which had puzzled earlier naturalists were now described in detail, and their origins made clear. Belemnites, thought to be thunderbolts in earlier days, were successfully interpreted as cephalopods by Erhart in 1724; echinoids were monographed by Klein in 1734, and coelenterates and other invertebrates by Buttner in 1714. By the time Linnaeus published his Systema Natura in 1735 fossils were treated and named as living things . Many eighteenth century naturalists continued to attribute the distribution of fossils to the action of a single flood, in spite of the difficulties of explain­ ing their relationship to strata and their regional variability. But others considered the explanation to be more complex. The belief grew that the Earth must be much older than the few thousand years of the traditional biblical chronology . c . L . Compte de Buffon (1707- 1788) showed by experiment that the Earth must have taken tens or even hundreds of thousands of years to cool from its molten origin to its present state . In Des Epoques de la Nature (1778) he described seven chapters of Earth history, the later ones characterized by the deposition of par­ ticular rock groups and populated by different animals and plants . Human history was relegated to the last and shortest of the epochs (Haber 1959) .

Eighteenth century advances

With the coming of the eighteenth century, the great fossils debate 'ran out of steam' in Britain. Hooke, Ray, Lister, and others were either dead or aged, and there were no naturalists of comparable stature in the younger generation. Further devel­ opments took place on the continent of Europe, in the first instance through the work of Johann Scheuchzer (1672 - 1733), a keen supporter of John Woodward. He translated Woodward's theory into Latin and argued strongly both for the organic origin of fossils and for the importance of Noah's Flood as a geological agent. Thus in Piscium Querelae et Vindiciae (1708) fossil fish themselves protested at

Early nineteenth century Paris

The problem of whether or not any animals had become extinct was tackled head on by Georges Cuvier (1769 - 1832), Professor of Anatomy at the Musee National d'Histoire Naturelle . He studied the skeletons of African and Indian elephants and showed that they were consistently different from each other, and should therefore be placed in dif­ ferent species . Both species were different from the bones of the mammoth from the gravels of Northern Europe, and from the mastodon of North America, which were nonetheless clearly elephants . Here at last was a demonstration of the former existence

540

6

Infrastructure of Palaeobiology

of species which surely were not still alive and unnoticed (Fig. 3) . As Cuvier's work progressed he described the remains of a whole zoo of extinct vertebrates : the giant sloth of South America, the mastodon of North America, a hippopotamus, rhinoceros, and so on. It seemed to him that the only possible cause for the extinction of this fauna was a sudden and wide­ spread 'revolution of the globe' . Cuvier had several lines of evidence for the nature of this event. He found a number of bones bearing attached oysters and other marine organisms, which suggested that the sea-level had risen, and the fact that beds con­ taining fossil bones tended to be in low-lying areas indicated that the waters had not covered the hill­ tops. Since many of his bones were well preserved, the flood could not have been violent enough to transport them very far, but had nonetheless been rapid enough to drown the animals where they stood (Rudwick 1972, Ch . 3) . Cuvier's colleague at the Museum, Jean Baptiste Lamarck (1744 - 1829), held a very different view of the history of animal life, and one that brought him into conflict with Cuvier. Lamarck worked in the Jardin des Plantes for many years, before taking over invertebrate animals at the Museum. He be­ lieved that the animal and plant kingdoms exhibited an endless series of gradations, and that classifi­ cation into species was only an artificial device . He believed that animals constantly changed their form as they reacted to changing environments. These changes continually moved them up a ladder of life which stretched from the lowly invertebrate at the

base to the mammals and man at the top . Extinction played no part in this scheme . Cuvier's ideas developed further as he came to study fossil bones from the gypsum quarries at Montmartre . When reconstructed, these appeared much less like living mammals than the bones from the gravels . Some combined characters from two or more living families, while others were quite un­ familiar . The key to the puzzle came as the stratigra­ phy of the Paris Basin was worked out and it was realized that the gypsum beds were older than the gravels . This stratigraphic work was carried out by Cuvier himself in association with Alexandre Brongniart (1770 - 1847) and published in the Journal des Mines in 1808 . In this monograph the strata above the Chalk were described in terms of their lithologies, and then subdivided with reference to the fossils they contained. A whole series of distinct faunas seemed to have appeared successively . In the Preliminary Discourse to his Recherches sur les Ossemens Fossiles de Quadrupedes (1812), Cuvier gave a general account of Earth history, based on his stratigraphic and palaeontological work, in which he showed that the generally quiet and tranquil conditions on Earth had been interrupted period­ ically by 'revolutions' of a type not seen at the present day; these had affected large areas of the world and had largely destroyed the existing fauna each time they occurred . Cuvier's ideas were accepted and developed by Adolphe Brongniart ( 1801 - 1876), Alexandre' s son. He published Historie des Vegetaux Fossiles (1828), in which four successive floras were distinguished.

Fig. 3 Skeleton of a mammoth discovered on the Lena River, Siberia, published by Georges Cuvier in Recherches sur Ies Ossemens FossiIes, 4th edn (18341 835, plate 1 1 ) .

6.5

541

History of Palaeontology

He made the point that there was a clear progression through these four floras, from the Carboniferous cryptogams, through the gymnosperms of the Mesozoic and the angiosperms of the Tertiary, to the varied plants of the present day. He related this progression, and the parallel one he saw in the animal record, to the gradual decrease in the level of carbon dioxide in the atmosphere, with changing climate and sea-level also having a secondary effect (Bowler 1976, Ch . 2) . Early nineteenth century Britain

Stratigraphic work was being carried out in Britain, at about the same time as in France, by a con­ temporary of Cuvier's, William Smith (1769 - 1839) . Smith was a land drainer, mineral surveyor, and canal engineer who lived in and around Bath in the west of England for much of his life . As early as 1796 Smith had realized that fossils could be used to identify strata more securely than lithology (Fig. 4) . He used this discovery to construct a table of strata

together with a sketch geological map of England and Wales in 1799, although only in 1815 was his great geological map published (Eyles in Schneer 1969) . His methods became widely known in England through the writings of John Farey, Joseph Townsend, and particularly James Parkinson (1755 - 1 824) . Parkinson was a London physician and one of the founders of the Geological Society in 1807. This Society was largely chemical and mineralogical in its earliest years, but rapidly took up stratigraphic studies using fossils until, by the mid-eighteen­ twenties, this was almost its exclusive concern. These studies, by men such as Thomas Webster, William Conybeare, and Gideon Mantell, were use­ ful contributions to the steadily growing store of regional geological knowledge, which almost inci­ dentally provided descriptions of previously un­ known fossils . With the work of Murchison in Wales and the Welsh Borders in the eighteen-thirties, a whole new invertebrate fauna was brought into view. The Geological Society eventually took over

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542

6 Infrastructure of Palaeobiology

from the Museum in Paris as the principal forum for palaeontological debate . Although William Smith was hailed as 'the father of English geology', the influence of Cuvier was also very strong. His ideas on the relationship of fossils to Earth history came to England through the translation of his Preliminary Discourse by Robert Jameson (1774- 1854) . The book was entitled Theory of the Earth, which linked it in people's minds with the earlier theories of Woodward and Ray. In his notes Jameson tied Cuvier's chronology to the Bible in a way that its author had never done . He ident­ ified Cuvier's final revolution with Noah's Flood, and emphasized the dramatic and destructive power of the events . In doing this he reflected the charac­ teristic theological slant of much British geology of this period. The leading exponent of the Deluge in Britain was William Buckland (1784 - 1856), Professor of Geology and Mineralogy at the University of Oxford (Fig. 5) . Although his main lines of evidence con­ cerned erratic plocks and the shape of valleys, he was strongly influenced by the researches he carried out on bone caves in Yorkshire and elsewhere . Kirkdale Cave was discovered in 1821 and inter­ preted by Buckland, after careful study of the living animals, as the den of hyenas, whose long occupancy was ended by the Deluge . Along with this emphasis on Biblical chronology came a belief that the Earth and everything in it was designed for man . Buckland viewed the history of life within this tradition in his Bridgewater Treatise (1836), putting forward not only the sort of progression that Brongniart had advocated but also the idea that God had a guiding hand in adapting life in the best possible way to changing conditions (Rupke 1983, Ch. 2) . It is a salutory reminder of the state of palaeon­ tological knowledge in the eighteen-thirties that another distinguished geologist and a pupil of Buckland, Charles Lyell (1797- 1875), could argue that there was no sign of progression in the fossil record . He appealed, like Darwin later, to the pov­ erty of collections and the lack of knowledge of many parts of the world, to show that negative evidence was no evidence . He made much of the discovery of mammals in the Oolitic rocks and of a reptile in the Devonian . He denied that early fossil fish, such as those found by Hugh Miller in Scotland, were any 'lower' than modern forms . This argument was used to back up his view that there was no evidence for the range of life, climate, environments, and geological processes ever being any different from those of the present day. Lyell also believed

Portrait of William Buckland published as the frontispiece to his Bridgewater Treatise, Geology and Mineralogy, 3rd edn (1858) . Fig. 5

_

that personal religious belief must be kept quite separate from the study of fossils or any other aspect of geology (Bartholomew 1976) . Many features of Lyell's geology appealed to Charles Darwin (1809 - 1882) . He read Lyell's Princi­ ples of Geology (1830 - 1833) while on the Beagle, and found it an excellent basis for interpreting the fea­ tures he saw on his voyage . Lyell befriended him on his return and gave Darwin entree to the Geo­ logical Society, where he met the experts he needed to work on his collections . Darwin's later writings on evolution, which were to influence all subsequent work on fossils, were not based on the study of the fossil record . In 1859 he was able, just like Lyell in 1830, to blame the inadequacy of the fossil record for not providing evidence to back up his theory. References Bartholomew, M. 1976. The non-progress of non-progression: two responses to Lyell's doctrine. The British Journal for the History of Science 9, 166- 174. Bowler, P.J. 1976. Fossils and progress : palaeontology and

6.5

History of Palaeontology

the idea of progressive evolution in the nineteenth century. Science History Publications, New York. Haber, F . C 1959 . The age of the world: Moses to Darwin . Johns Hopkins Press, Baltimore. Porter, R. 1977. The making of geology: Earth science in Britain 1 660 - 1 815. Cambridge University Press, Cambridge. Raven, CE. 1942 . John Ray, naturalist. His life and works . Cambridge University Press, Cambridge. Rudwick, M.J.5. 1972. The meaning of fossils: episodes in the history of palaeontology. Macdonald, London . Rupke, N.A. 1983 . The great chain of history: William Buckland and the English school of geology (181 4 - 1 849). Clarendon Press, Oxford. Scherz, G. 1958 . Nicholaus Steno's life and work. Acta Historica Scientiarum Naturalium Medicinalium 15, 9 - 86. Schneer, CJ. (ed .) 1969 . Towards a history of geology . M.I.T. Press, Cambridge, Ma . Torrens, H . 5 . 1985 . Early collecting in the field of geology. In: O. Impey & A. Macgregor (eds) The origins of museums, pp. 204-213. Clarendon Press, Oxford .

6 . 5 . 2 Darwin to Plate Tectonics P . J . BOWLER

Introduction

Fossil discoveries continued apace in the late nine­ teenth century, but the theoretical foundations of palaeontology were transformed by the advent of evolutionism . For several decades the attempt to reconstruct the development of life on Earth using fossil and other evidence was the most active area of evolutionary biology, although this programme encouraged a distinctly non-Darwinian view of how the process worked . In the twentieth century palae­ ontologists somewhat belatedly adapted to the syn­ thesis of Darwinism and genetics, and began to grapple more actively with the geographical dimen­ sion - although for many years they opposed the theory of continental drift. New discoveries, 1860 - 1940

The impetus given to fossil collecting in the early nineteenth century was sustained in later decades by more extensive mining activities and by the opening up of new areas of the Earth to scien­ tific exploration . In Europe and America major new

543

museums were founded to exhibit and interpret the discoveries to the public and as centres of research. The British Museum (Natural History) in London and the American Museum of Natural History in New York are obvious examples of museums that built up their reputations at this time . By the early twentieth century many large cities had similar ins titutions, giving rise to considerable rivalry in the establishment of good collections . Many of the new discoveries helped to fill in the outline of the history of life created by Cuvier and his followers, greatly extending knowledge of the dinosaurs and other groups which had originally been established on the basis of small numbers of incomplete speci­ mens . The popularity of evolution theory focused particular attention on fossils that could be ident­ ified as 'missing links', again fuelling the rivalries of collectors and institutions . The Miocene fauna of Pikermi, Greece, was studied by Albert Gaudry in the eighteen-sixties . His work threw new light on the proboscidean Deinotherium and on many other forms, leading Gaudry to support the concept of a continuous evol­ utionary development linking the known Eocene and Pleistocene faunas (Rudwick 1976; Buffetaut 1987) . The discovery of an Archaeopteryx specimen with feathers at Solnhofen, Bavaria, in 1861 aroused intense excitement, especially after it was acquired (at vast expense) by the British Museum (Natural History) and subsequently described by T.H. Huxley as an intermediate between reptiles and birds . A second specimen was discovered in 1877. The unearthing of almost complete Iguanodon speci­ mens at Bernissart, Belgium, in 1878 showed that these dinosaurs were bipedal, not quadrupedal as originally reconstructed (Colbert 1971 ) . A mounted specimen in Brussels gave a new awareness of the appearance of dinosaurs from 1883 onwards . Other important collections of fossil reptiles came from the Jurassic Oxford Clay of Peterborough in Cambridgeshire and from Transylvania, the latter studied by the colourful and eccentric baron Franz Nopsca. In North America, the opening up of the West led to a veritable 'war' between collectors such as O . c . Marsh and E . D . Cope . Their discoveries o f Jurassic dinosaurs from Colorado in the eighteen-seventies greatly extended knowledge of the 'Age of Reptiles' and formed the basis of impressive museum dis­ plays . Marsh's discovery of toothed birds in Kansas supported the evolutionary link already suggested by Archaeopteryx (Fig . 1). Marsh also collected a series of fossils in Nebraska throwing light on the

544

6 Infrastructure of Palaeobiology

'1l0CENE.

i\liohiPPll8 (AIu:h.ithtriU?l').

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Fig. 1

evolution of the modern horse, culminating with the four-toed 'Eohippus' in 1876 . The fossil sequence was described as 'demonstrative evidence of evol­ ution' by T.H. Huxley (Fig. 2) . In the early twentieth century, H . F . Osborn described gigantic early mammals from the American west, including the titanotheres . O f particular interest t o the public were fossils relating to the origin of mankind (Reader 1981) . In 1857 the discovery of a cranium at Neanderthal in Germany arous e d much controversy but was eventually accepted as an early human form with some ape-like characters (Fig. 3) . For some time con­ sidered as a possible ancestor of modern humans, the neanderthals were reinterpreted in the early twentieth century by Marcellin Boule, Arthur Keith, and others as a parallel and distinct human family driven to extinction by our own forebears . Eugene Dubois' discovery of 'Pithecanthropus erectus' (now Homo erectus) in Java during the eighteen-nineties revealed an even earlier human form, again dis­ missed by many as a side-branch of our family tree . Thinking on human origins was to some extent thrown off course by the notorious Piltdown fraud of 1912, in which a human cranium and an ape jaw were attributed to an intermediate 'Eoanthropus' . This reinforced the generally popular assumption

Fig. 2 Modification of the teeth and lower limbs of the horse family, after Marsh . (From Wallace, A.R. 1 889 . Darwinism. Macmillan, London, p. 388) .

Fig. 3 The neanderthal cranium. (From Huxley, T.H. 1863 . Man 's place in Nature. Williams and Norgate, London, p. 139 . )

6 . S History of Palaeontology that the expansion of the brain was the chief driv­ ing force of human evolution, making it easier to dismiss Pithecanthropus, with its small brain and upright posture, as irrelevant. Raymond Dart's dis­ covery of the first australopithecine at Taungs, South Africa, in 1924 was again dismissed because of the refusal to admit that a small-brained hominid could have achieved bipedalism. Dart was also ignored because of the widespread opinion that mankind must have evolved in central Asia, not Africa (al­ though expeditions to Asia did reveal more Homo erectus specimens, at first known as Sinanthropus or Peking man) . The australopithecines only began to be taken seriously after Robert Broom's discoveries of the nineteen-thirties . Palaeontology and evolution theory

The search for 'missing links' ensured that evol­ utionism gave an added zest to fossil hunting, but it would be a mistake to overemphasize the impact of Darwin's theory on palaeontology . The description of fossils was still seen as a branch of morphology, with little attention being paid to intraspecific vari­ ation or the possibility of local effects on popu­ lations . Palaeontologists were thus not in the best position to appreciate the most original aspects of Darwin's theory. They had, in any case, begun to look for patterns of development in the fossil record long before the Origin of species appeared in 1859. The element of discontinuous change stressed by early catastrophists had begun to decline in the eighteen-fifties . H . G . Bronn and Richard Owen had begun to emphasize that there were 'laws of devel­ opment' to be seen linking the fossils within each class, while the general idea of progressive evolution had been circulated as early as 1844 by Robert Chambers in his popular and controversial Vestiges of the natural history of Creation (Bowler 1976) . It was recognized that the development of life included branching and what is now called adaptive radi­ ation, but there was a preference for depicting the 'tree of life' with a central trunk leading through to the human race as the pinnacle of creation . The debate sparked off by Darwin's Origin certainly catalysed the scientific community's conversion to evolutionism, but the impetus for most palaeon­ tological evolutionism came from transformations within the 'developmental' view of life's history already taking shape in the pre-Darwinian era. A few important figures, of whom J.W. Dawson of Montreal is the best example, continued to promote a discontinuous and hence anti-evolutionary view of

545

the fossil record . But in general the acceptance of a loosely-defined evolutionism came naturally to most palaeontologists, for whom the new approach was little more than an extension of the earlier search for abstract laws of development. Many evolutionists saw their principal task as the reconstruction of the history of life on Earth using the fossil record, supplemented by evidence from comparative anatomy and embryology. In Germany, Ernst Haeckel popularized this version of 'Darwinism' in books such as his History of Creation (1876) . Even T.H. Huxley only began to make active use of evolutionism in the study of fossils after reading Haeckel - his original support for Darwin was purely tactical (Desmond 1982) . Palaeontol­ ogists now began to arrange the known specimens of each group into the most plausible evolutionary series, and of course to look for the missing links . Haeckel's recapitulation theory - the claim that ontogeny recapitulates phylogeny - was widely accepted by palaeontologists looking for clues as to the 'shape' of the pattern they should expect to find . In these circumstances, it is hardly surprising that many of their views on the mechanism of evolution were distinctly non-Darwinian in character. Haeckel himself was a Lamarckian, recognizing that the inheritance of acquired characters provided a bet­ ter theoretical basis for recapitulation than natural selection. Many so-called 'Darwinists' might be bet­ ter called pseudo-Darwinists, since their commit­ ment was to evolutionism rather than to natural selection. In the later nineteenth century many palaeontologists became actively opposed to the selection theory (Bowler 1983, 1986) . In America, an active school of neo-Lamarckism flourished from the eighteen-seventies onwards, led by the verte­ brate palaeontologist E . D . Cope and the invertebrate palaeontologist Alpheus Hyatt. They too supported recapitulation and claimed that evolution occurred by regular extensions to the process of individual growth . Arrangements of fossils into apparently linear sequences, as in the case of the horse family (Fig. 2) helped to create an impression that evolution was too regular a process to be explained in terms of random variation and selection. The fascination with 'laws of development' led many biologists to reject Darwin's claim that adap­ tation was the chief guiding force of evolution. They believed that factors internal to the organism would drive variation in a particular direction what­ ever the demands of the environment. On this model, one could expect parallel lines of evolution to advance steadily in the same direction over vast

6 Infrastructure of Palaeobiology

546

periods of time . In Britain such a view was ex­ pounded by Owen's disciple St. George Mivart, who became one of Darwin's most active critics . Nor were Owen and Mivart mere speculators, since they recognized the possibility of mammal-like reptiles ahead of Huxley . Many palaeontologists supported the concept of orthogenesis (parallel evolution) driven by internal forces . Hyatt's arrangements of fossil cephalopods were widely accepted as classic examples of nonadaptive evolution. Vertebrate palaeontologists thought that many extinct species had developed grossly maladaptive characters be­ fore finally succumbing, one example being the antlers of the 'Irish elk' . Such ideas were still being promoted through into the nineteen-thirties by emi­ nent palaeontologists such as H .F . Osborn . Osborn's subordinates at the American Museum of Natural History - including W . D . Matthew and W.K. Gregory - tried to sustain less extreme anti­ Darwinian positions, but were still in a minority. It would be easy to dismiss the palaeontologists' support for non-Darwinian concepts such as recap­ itulation, Lamarckism, and orthogenesis, as an aberration in the history of evolutionism, but this is a misconception engendered by our modern prefer­ ence for the selection theory. In the late nineteenth century, non-Darwinian palaeontologists were in the forefront of evolutionary research, and they helped to shape the popular conception of what

evolutionism is all about. Their views were in­ strumental in circumventing the application of Darwinian principles to human origins : no one thought of specifying an adaptive scenario to ex­ plain why humans separated from apes, since it was assumed that the primates were governed by an inherent trend toward brain-growth. The popu­ larity of parallel evolution helped to ensure that many hominid fossils were dismissed as the pro­ ducts of independent lines of evolution unconnected with our own origins . Such views remained accept­ able to palaeontologists and palaeoanthropologists well into the twentieth century, long after they had been overtaken by changing attitudes elsewhere in biology (Bowler 1986) . The emergence of genetics at the turn of the century ensured that most experimental biologists soon came to repudiate Lamarckism, but palaeon­ tology remained a morphological discipline and resisted the new trends . The 'Mendelian revolution' would eventually complete what Darwin had been unable to achieve : the destruction of the develop­ mental world view characteristic of nineteenth-cen­ tury morphology. But not until the nineteen-forties did palaeontologists begin seriously to take note of the new developments . It was G . G . Simpson's Tempo and mode in evolution of 1944 that forced the discipline to confront what has become known as the modern synthetic theory of evolution. The re-

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Fig. 4

6.5

547

History of Palaeontology

sult was a transformation in the kind of questions studied by palaeontologists in the postwar era. Parallelism and orthogenesis were replaced by adaptive scenarios and a greater concern for micro­ evolution in local populations .

ontologists had to respond. Land bridges were abandoned and the continental movements postu­ lated by geologists have become major features of our current explanations of the evolution and distribution of life on Earth .

Palaeontology and geography

References

Although nineteenth-century palaeontologists were chiefly concerned with the creation of patterns of evolutionary development, their increasing knowl­ edge of the world-wide distribution of fossils forced them to grapple with the geographical per­ spective . Darwin's theory drew attention to the apparently anomalous distribution of some modem forms and explained the phenomenon as the result of migrations in earlier geological epochs. Biogeo­ graphers postulated 'land bridges' in the past joining various parts of the Earth's surface . Palae­ ontologists also began to make use of this concept - Haeckel, for instance, suggested that the lack of fossil hominids could be explained by assuming that our ancestors had lived on the lost continent of Lemuria, now sunk in the Indian Ocean. When it was recognized that the Palaeozoic faunas of South America and South Africa were identical, it was natural to postulate a land bridge across the Atlantic which had sunk in the Mesozoic to allow the two continents' faunas to diverge . In thus ignoring the possibility of continental movement, palaeontol­ ogists merely followed the lead given by physical geologists . Thinking on the geographical distribution of ­ life in the Tertiary was deeply influenced by the Canadian-American palaeontologist W. D . Matthew, whose Climate and evolution of 1914 took the per­ manence of the existing continents for granted. Matthew saw central Asia as the heartland of mammalian evolution, from which waves of suc­ cessively higher forms spread out to the rest of the world (Fig. 4) . This theory was even extended to human origins, generating a widespread reluctance to take the discovery of hominid fossils in Africa seriously . When the possibility of continental drift was proposed by Alfred Wegener and a handful of followers, palaeontologists were in the forefront of opposition during the nineteen-twenties and nine­ teen-thirties . Charles Schuchert, in particular, de­ fended the traditional concept of land bridges . Even C . C . Simpson wrote actively against continental drift in the nineteen-forties . The advent of plate tectonics in the postwar years thus represented a second major theoretical revolution to which palae-

Bowler, P.J. 1976 . Fossils and progress: palaeontology and the idea of progressive evolution in the nineteenth century. Science History Publications, New York. Bowler, P.J. 1983. The eclipse of Darwinism: anti-Darwinian evolution theories in the decades around 1 900. Johns Hopkins University Press, Baltimore. Bowler, P.J. 1986 . Theories of human evolution: a century of debate, 1 844 - 1 944. Johns Hopkins University Press, Baltimore & Basil Blackwell, Oxford. Buffetaut, E . 1987. A short history of vertebrate palaeontology. Croom Helm, London. Colbert, E.H. 1971 . Men and dinosaurs . Penguin Books, Harmondsworth . Desmond, A. 1982 . Archetypes and ancestors: palaeontology in Victorian London, 1 850 - 1 875 . Blond & Briggs, London . Reader, J. 1981 . Missing links: the hunt for earliest man . Collins, London. Rudwick, M.J.S. 1976. The meaning of fossils: episodes in the history of palaeontology, 2nd edn . Science History Publications, New York.

6 . 5 . 3 Plate Tectonics to Pa leo bio logy

J . W . VALENTINE

Introduction

During the period 1960 - 1975, palaeontology underwent a vigorous and lasting expansion of concerns and goals . While some of the roots of this expansion lay in earlier times, the formalization of concepts and the definition of problems that have grown into major features of palaeontological re­ search occurred during this period . From its incep­ tion as a science, palaeontology has drawn upon both geological and biological sciences, and its findings have been applied to problems in each of those fields . It is thus appropriate briefly to mention major trends and events in biology and geology that became of particular importance to palaeontology.

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Trends in earth science

The period was dominated by the rise of the plate tectonic paradigm (for a short historical account see Hallam 1973) . Scattered but inconclusive evidence that the continents had held different geographical relations in the past had been adduced over several decades, but in the nineteen-fifties palaeomagnetic studies provided strong support for this hypothesis . Then in the nineteen-sixties the basis of differential movements of crustal segments was clarified . Hess (1962) suggested that oceanic crust was generated at deep ocean ridges and consumed in trenches, and palaeomagnetic studies of the sea floor soon pro­ vided supporting evidence . There followed a flood of geophysical experiments and observations lead­ ing to the development of the theory of plate tecton­ ics by the close of the nineteen-sixties . During this period also, the need was felt for direct exploration of the ocean floor, and in 1964 a major initiative was launched to take deep cores of that floor (Joint Oceanographic Institutions for Deep Earth Sampling - JOIDES) . This project led to the estab­ lishment of the Deep Sea Drilling Program (DSDP), the Reports from which had reached volume 27 by the close of 1974 . The results of the drilling pro­ gramme supported the implications of the geo­ physical data. Continents, continental fragments, and islands had ridden with the moving sea floor plates in which they were embedded . By 1973 many features of the relative positions of major continental masses were well enough worked out for palaeo­ geographic maps that covered most of Phanerozoic­ time (Smith et al. in Hughes 1973) to be constructed .

Trends in life science

Developments that affected palaeontology included a great rise in interest in the ecological disciplines, fuelled in part by concern over man's impact on the environment. Field exploration and experimen­ tation were enlarged and extended into ecosystems, such as the pelagic and deep-sea realms, which had been poorly known and indeed misunderstood. Studies were particularly intense on factors regulat­ ing the ecological and evolutionary controls affect­ ing the demography and distribution of natural populations, and on the principles that regulate the stability and diversity of ecosystems . Evolutionary studies were much concerned with processes of genetic change within lineages, and with speciation (e . g . Mayr 1963; Dobzhansky 1970) and with the

significance of neutral mutations in evolution (see Kimura 1983); and a beginning was made in evol­ utionary aspects of development from a molecular perspective (Britten & Davidson 1971 ) . Early history o f life

Palaeontology in 1960 - 1975 flourished in response to its own traditional concerns and at the same time was increasingly influenced by contemporary events in earth and life sciences . Among the out­ standing examples of palaeontological research were those which illuminated the fossil record of Archaean and Proterozoic life and of the earlier metazoan radiations . During the nineteen-sixties it became generally appreciated that stromatolites dating from the Archaean were marine algal struc­ tures . In 1965 a microbiota of presumed prokaryotes was described from the Gunflint Iron Formation, about two billion years old, which began a series of studies that revealed a microbial record extending back well into the Archaean (Section 1 .2) . This led to important syntheses of the geological and palaeon­ tological evidence of Precambrian environments . A major element in the resulting hypotheses was that biogenic oxygen levels, representing a balance be­ tween supply via photosynthesis and consumption via oxidation of iron and other reduced substances, had risen across a variety of critical concentrations during the Proterozoic to permit the evolution of increasingly complex and active organisms . The appearance of soft-bodied metazoan fossils in Late Precambrian rocks in the Ediacara Hills, South Australia was confirmed and the fauna de­ scribed . Faunas in Europe, Africa, Asia, and North America, some known earlier and some now de­ scribed, were identified as being similar to the Ediacaran assemblage, and the concept of a Late Precambrian metazoan fauna spanning perhaps 100 million years became established (Section 1 . 3) . At the same time, it was proposed that there was a fauna, consisting chiefly of small enigmatic fossils, many phosphatic, that followed Ediacaran time but preceded the appearance of trilobites and echino­ derms in the Early Cambrian. Elements of this fauna had long been known, but its distinctive position became clarified through descriptions of late Pre­ cambrian- Cambrian sections in Siberia and by synthesis of this stratigraphic data with records from Europe (Sections 1 .4, 5 .2 . 5) . Also during the late nineteen-sixties and early nineteen-seventies, the soft-bodied fauna of the Burgess Shale of British Columbia was recollected and opened to restudy

6.5

History of Palaeontology

and re-evaluation; it proved to be far less clearly allied to living taxa than had been supposed (Section 3 . 1 1 .2) . From these studies the early history o f life began to be written; life extended billions of years back in time, presumably beginning in an essentially anoxic environment. A radiation of soft-bodied metazoans preceded Cambrian time (Section 1 .3), but never­ theless the abrupt appearance of metazoan phyla during the Early Cambrian did not appear to be an artifact, but to represent a true evolutionary episode of singular magnitude, producing many novel body plans . Systematics and biostratigraphy

Researches on mineralized skeletal fossil groups of the Phanerozoic continued apace, with noteworthy activity in early Palaeozoic echinoderms, Permian brachiopods, early fishes, and taxa involved in the reptile - mammal transition. The organization and revision of scattered systematic and stratigraphic data into multivolume treatises, begun in previous years, continued, and these data were subjected to a further level of summarization in reviews of geo­ logical ranges of taxa, with assessments of changing diversifications, extinctions, and standing diversity levels, especially those of higher taxa in terms of their familial representation (Harland et al . 1967) . Critical reviews of the methodology and application of biostratigraphy signalled increasing rigour in this area. Practical advances in biostratigraphy in­ cluded the major refinement of zonations of late Mesozoic and Cenozoic rocks arising from study of micro- and nannofossils recovered from DSDP cores. Palaeoecology and palaeobiogeography

Against this background of intense activity along well established trends, palaeontological subdis­ ciplines that were in their infancy grew into major fields . Palaeoecology (Section 4) and palaeobio­ geography (Section 5 . 5) are outstanding examples . As both industrial and academic programmes were employing palaeoecologists, a stream of students trained in biological as well as geological sciences was attracted to palaeontology, and many of the students had ecological interests . Early work focused on environmental reconstructions, thus contribut­ ing to geological interpretations; there was, how­ ever, growing interest in population and community palaeoecology and biogeography. Fossil assem-

549

blages were increasingly appreciated as represent­ ing the remains of biotic communities, and their description in this light tended to bring them to life and to fill them with new interest. Accordingly the interpretation of palaeocommunities and their palaeoenvironmental contexts became a common research goal, and the burgeoning literature of population and community biology was co-opted to serve as the basis for many theoretical aspects of the fossil record (e . g . Shopf 1972; Valentine 1973) . Trace fossils, reflecting as they do the activities of organ­ isms, proved to be sensitive environmental indi­ cators of special importance, for they commonly occur in sediments otherwise devoid of fossils, and ichnology grew into a thriving subdiscipline (Sections 4 . 1 1, 4. 19.4, 4. 19.5) . Still another branch of palaeontology expanded with the study of nanno­ fossils and microfossils from DSDP and other deep­ sea cores. The cores yielded planktic forms from surface and near-surface waters and benthic forms from the deep-sea benthos . Subjected to palaeo­ ecological, biogeographical and isotopic analyses, these fossils permitted reconstruction of ancient ocean climates, current systems, biological pro­ ductivity, and other features which contributed to the rise of the discipline of palaeoceanography. The advent of plate tectonic theory provided a basis for the reconstruction of palaeobiogeographies that resembled historical reality on a global scale more or less throughout the entire Phanerozoic. The result was startling. Biodistributional patterns that had been attributed to either dispersal across 'land bridges' and 'stepping stones' (e . g . to bridge the early Mesozoic Atlantic Ocean), or to narrow bio­ distributional barriers between distinctive faunas (e . g . to explain the juxtaposition of American and European-type assemblages in the Early Cambrian of Northeastern America), were suddenly clarified . The 'land bridges' a s envisioned did not exist, but rather the continents themselves had been juxta­ posed during the Early Mesozoic; and the Cambrian barrier had once been an ancient ocean, long since subducted (see also Section 5 . 12) In addition to solving biodistributional puzzles of this sort, palaeogeographical reconstructions implied that environmental conditions, marine and terrestrial alike, must have varied in response to plate tectonic processes. Islands, continental fragments, and entire continents had moved between climatic zones and had been variously aggregated and dispersed . Not only would the climates of mobile geographical elements change as they entered new latitudes, but the climates themselves, and the circulation patterns

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of atmosphere and ocean, would be affected . Dis­ tributional and associational patterns in the fossil record could now be placed in environmental con­ texts by evidence independent of the fossils them­ selves, and palaeoecology could now be concerned not only with the interpretation of local assem­ blages, but also with their contexts in regional and global patterns (Hughes 1973) . It became possible in principle not only to apply and test theoretical notions from population and community ecology to fossils, but to formulate and test theoretical prin­ ciples from fossil evidence . Evolutionary studies

The growing confidence in applications of fossil data to biological theory was also exemplified in evolutionary studies . The patterns of morphological change observed among fossils did not always meet the expectations of many evolutionary models, and Eldredge & Could in Schopf (1972) proposed that morphological changes within evolving lineages were concentrated at morphospeciation events, and that between such events change was slight - an alternation of morphological change and stasis that they termed 'punctuated equilibrium' . As these authors pointed out, long-term trends in morpho­ logical change could be attributed to the differential success of lineages that happen to exhibit change in a particular direction favoured by subsequent events, and need not indicate a history of phyletic evolutionary trends . Furthermore, the abrupt ap­ pearance of higher taxa in the record might indicate a punctuational origin . As for the fate of higher taxa, the accumulated data of their waxing and waning over Phanerozoic time led to studies of fossil taxonomic diversity (Section 5 . 3) and to theor­ etical models to account for their observed behav­ iours and for evolutionary change in general . In the Red Queen hypothesis (Section 2 .5), for example, it was argued that adaptive improvement in a given lineage must perforce reduce adaptation in others, and when evolutionary processes acted to over­ come this disadvantage, they produced adaptive deterioration in still other lineages; thus evolution must occur merely to maintain the status quo . From such hypotheses, the field of macroevolution was reborn within palaeontology. As the concerns of palaeontology broadened, text­ books appeared that stressed these new interests (e . g . Raup & Stanley 1971) and new professional journals were established (Palaeogeography, Palaeo­ climatology, Palaeoecology, from 1965; Lethaia, from

1968) that featured palaeobiological contributions . The journal Paleobiology appeared in 1975, marking the close of this period. During 1960 - 1975, palae­ ontology had become vastly enriched and diversi­ fied in a virtual 'evolutionary radiation' and within its many branches lay the potential for further fruitful expansion. References Britten, R.J. & Davidson, E . H . 1971 . Repetitive and non­ repetitive DNA sequences and a speculation on the origins of evolutionary novelty. Quarterly Review of Biology 46, 1 1 1 - 138. Dobzhansky, Th . 1970. Genetics of the evolutionary process . Columbia University Press, New York . Hallam, A. 1973. A revolution in the earth sciences. Clarendon Press, Oxford . Harland, W.B. et al. 1967. The fossil record. Geological Society of London, London. Hess, H . H . 1962 . History of ocean basins. In : A.E.}. Enge!, H . L . James & B . L . Leonard (eds) Petrologic studies: a vol­ ume in honor of A.F. Buddington, pp . 599 - 620 . Geological Society of America, Boulder, Co. Hughes, N.F. (ed. ) 1973 . Organisms and continents through time. Special Papers in Palaeontology, No. 12. Kimura, M . 1983 . The neutral theory of molecular evolution . Cambridge University Press, Cambridge. Mayr, E . 1963 . Animal species and evolution . Belknap Press, Cambridge, Ma. Raup, D . M . & Stanley, S .M. 1971 . Principles of paleontology. Freeman, San Francisco. Schopf, T.J.M. (ed . ) 1972. Models in paleobiology. Freeman, Cooper, San Francisco . Valentine, J.W. 1973. Evolutionary paleoecology of the marine biosphere. Prentice-Hall, Englewood Cliffs, NJ .

6 . 5 . 4 The Past Decade and the Future A . HOFFMAN

Introduction

The scope of palaeontology is very broad, for it covers the entire history of life on Earth. Therefore, the spectrum of research strategies must also be very wide. During the nineteen-seventies, however, a gap appeared (and has continued to grow in the nineteen-eighties) between two major approaches to palaeontology. On the one hand, the traditional

6 . S History of Palaeontology approach - palaeontography - tends to emphasize the description of fossils and the reconstruction of extinct life as the basis for establishing a classifi­ cation of organisms that reflects their phylogeny. The description of fossils and their distribution in the rocks is obviously important also for biostra­ tigraphic correlation. On the other hand, many palaeontologists have boldly undertaken to search for general rules that may govern the causal pro­ cess(es) responsible for the pattern of life, or the appearance and order of the biosphere . In this ap­ proach - which might be called theoretical palaeo­ biology the empirical data of palaeontology are primarily employed for generating and testing theoretical hypotheses about the laws of organic and biotic evolution. The growing gap between palaeontography and theoretical palaeobiology has been the most conspicuous feature of the last decade in the history of palaeontology, but it must be closed in the future . -

551

extant? What was the ecological and biogeographi­ cal structure of the biosphere in the geological past? To answer such questions using palaeontological data requires a methodology of historical recon­ struction. This is the subject of the ongoing theor­ etical debates in palaeontography: the paradigm method of functional morphology versus construc­ tional morphology in the reconstruction of organ­ isms (Section 4. 1), cladistic versus stratophenetic methods in the reconstruction of phylogeny (Section 5 . 2), etc. The rival methodologies refer also to con­ trasting perspectives on various problems in evol­ utionary biology: the relative roles of selection and constraint in phenotypic evolution (Sections 2.2, 2.3), the commonness of convergent and parallel evol­ ution, etc. Thus, the palaeontographical approach to the history of life cannot be separated from theor­ etical considerations; yet within its conceptual framework, theory is not a goal in itself. Theoretical palaeobiology

Palaeontography

That the palaeontographical approach is here re­ garded as traditional does not imply that such re­ search is conducted today in the same way as it was in the last century, or even 20 years ago . New analytical tools have come into common use : elec­ tron microscopy, biogeochemistry, mineralogy, and even crystallography of fossils, etc. Incomparably more attention has been paid recently to the func­ tional morphology of extinct organisms . The geo­ logical setting of fossils has also come more into focus, as recent developments in sedimentology allow quite detailed information about the habitat of extinct organisms to be deduced from the rock record. Palaeocommunity analysis has reached its peak as the means of describing the biotic environ­ ment of life forms in the geological past. In spite of such innovations and shifts in emphasis, however, the major achievements of this research strategy could conceivably have been made 20 years ago: discovery of the conodont animal, reinterpretation of many Ediacaran fossils, reconstruction of tabu­ lates as sponges rather than corals, etc. Perhaps even more importantly, the main questions being asked within the conceptual framework of the palaeontographical approach have remained largely the same as before : What did extinct organisms look like, and how did they live? What is the shape of 'the tree of life' which links together the gen­ ealogies of all organic groups, both extinct and

Just the opposite is the case with theoretical palaeo­ biology . In this approach, the emphasis is on the questions : Why is the shape of 'the tree of life' as it is? How does the process of evolution operate? What are the universal laws of organic and biotic evolution? The approach is therefore distinctively nomothetic. These questions are certainly not new; they were not posed for the first time in the nineteen-seventies . Palaeontology at an earlier peak (at the turn of the century and even well into the second quarter of the twentieth century) largely focused on these problems . Abel, Cope, Hyatt, Osborn, Wedekind, and Schindewolf all followed the nomethetic approach, regarding the fossil record primarily as the main source of empirical data rel­ evant to these questions - at a time when the term palaeobiology was first coined . But the method­ ological rigour of modern theoretical palaeobiology, with its emphasis on pattern recognition and expla­ nation through quantitative modelling and hypoth­ esis testing, is entirely new. The beginnings of this research strategy can be traced back at least to Brinkmann (1929) but the onset of its explosive development is symbolically represented by the appearance of Schopf's Models in paleobiology (1972) and the founding of the journal Paleobiology in 1975 . In retrospect, these publishing events seem to have been crucial in shaping the research area of theoretical palaeobiology. Since about 1975, the research effort of theoretical palaeobiology has been primarily organized around

552

6 Infrastructure of Palaeobiology

four subject areas of major controversy (for re­ view and references see Hoffman 1988) . In each case, the controversy chiefly concerned a proposal that some specifically macroevolutionary pro­ cesses - irreducible to the microevolutionary pro­ cesses envisaged by the neo-Darwinian paradigm of evolution - are responsible for the origin of the macroevolutionary patterns described by palaeobiologists .

1 Punctuated equilibrium. The concept of punctuated equilibrium seems to have attracted most attention,

among palaeontologists as well as among other scientists and the general public. Perhaps the main cause for the heated debate on punctuated equilib­ rium has been the ambiguity of and repeated changes in the meaning of this concept since its original formulation by Eldredge & Gould in Schopf (1972) . Its proponents and advocates have presented and argued for quite a number of substantially different versions (sometimes more than one within the body of a single article) . In its 'weak' version, punctuated equilibrium is primarily meant as a contrast to so-called phyletic gradualism (i. e . the view that phenotypic evolution proceeds continu­ ously in the same adaptive direction and at a con­ stant rate) . Punctuated equilibrium then means that the rate and direction of phenotypic evolution vary along a considerable proportion, or even an over­ whelming majority, of phyletic lineages . When so understood, punctuated equilibrium is entirely triv­ ial because this has never - since the advent of the neo-Darwinian paradigm - been seriously doubted by evolutionary biologists or palaeontologists . The 'strong' version of punctuated equilib­ rium includes two assertions: (1) that phenotypic evolution never proceeds gradually, or that no sig­ nificant evolutionary change is achieved by ac­ cumulation of small adaptive steps; and (2) that all phenotypic evolution is associated with speciation events . This latter assertion cannot be tested in the fossil record because, apart from a few instances of indisputable lineage splitting, speciation must be equated in palaeontology with considerable pheno­ typic change . The first assertion, however, has been repeatedly tested and refuted. In spite of a myriad of empirical problems, several cases of significant gradual evolution have been convincingly docu­ mented (Section 2 . 3) . An even more radical variant of this 'strong' version of punctuated equilibrium is nevertheless tenable : that even an apparently con­ tinuous sequence of fossil populations may in fact consist of a discontinuous series of extinct species,

because continuity is always assumed rather than proven . This variant, however, explicitly enters the realm of metaphysics . The 'moderate' version of punctuated equilibrium emphasizes the occurrence, and even commonness, of stasis in the evolutionary history of each phyletic lineage . When stasis is understood as the complete evolutionary stasis of the entire phenotype, this proposition is untestable because the fossil record provides data concerning only a small sample of anatomy while evolution may as well occur in soft­ body anatomy, physiology, or behaviour. When stasis is understood to be the absence of change in some morphological characters, it certainly appears to be a widespread phenomenon. It may be due to a variety of microevolutionary processes, and it then perfectly fits the neo-Darwinian paradigm. To emphasize this phenomenon borders upon trivi­ ality. In principle, stasis may also be due to some constraints on morphological evolution which ac­ tively resist a change favoured by natural selection. The claim, however, that this is in fact the main mechanism of morphological stasis is unsupported by any evidence . Thus, the debate on punctuated equilibrium has not led to the finding of any new evolutionary rules . It has, however, considerably raised the standards of palaeontological research on evolutionary rates and produced much fascinating empirical data on phenotypic evolutionary rates in a wide variety of fossil organisms . 2

Species selection . The results of the controversy on species selection are quite different. Since its first

formulation (Stanley 1975) the concept of species selection has evolved as much as punctuated equi­ librium, with which it was initially linked (Section 2.6). It is clear by now, however, that if species selection is meant to designate something more than just a net effect (on the supraspecific level) of natural selection at the individual level, then it must be defined as a causal process changing the relative speciosity of various clades due to selection for or against their heritable species-level prop­ erties. It also must be distinguished from species drift, i . e . the accidental change in species richness of various clades due to the vagaries of their en­ vironment or pure chance . Under such a definition, species selection is not related at all to punctuated equilibrium. It indeed represents a macroevolution­ ary process that can, potentially, operate in nature, but not one actual example of species selection has yet been convincingly documented . The debate on

6 . S History of Palaeontology species selection has thus resulted in expanding the scope of potential evolutionary forces which can, in theory, be invoked to explain macroevolutionary patterns, but the empirical research it stimulated has not been particularly productive .

3 Taxonomic diversification. Much palaeobiological discussion has been devoted to the problem of taxonomic diversification of the biosphere in the Phanerozoic . The very nature of the fossil record makes it difficult to establish the empirical pattern of change in global taxonomic diversity through geological time (Section 2 . 7) . Assuming, however, that this pattern can be at least approximately represented by a global-scale compilation of the stratigraphic ranges of taxa at a supraspecific level, and at the time resolution of the geological stage, Sepkoski (1978) undertook a bold attempt at its causal explanation by a deterministic model . A var­ iety of theoretical models have been subsequently proposed to account for these empirical data. Sepkoski's more complete equilibrium model of diversity-dependent diversification of three great evolutionary faunas which have displaced one another via biotic interactions seems to have at­ tracted most attention (Section 1 .6) . However, a nonequilibrium model envisaging diversity­ dependent diversification as driven by evolutionary novelties and mass extinctions may withstand the test of empirical data even better. These models explain the macroevolutionary pattern of taxonomic diversification in the Phanerozoic by reference to a set of specifically macroevolutionary rules, operating at a supraspecific level of biological or­ ganization. However, a simple stochastic model rep­ resenting the pattern of taxonomic diversification as a net result of two independent random walks one concerning the average rate of speciation, the other the average rate of species extinction per geological state - cannot be rejected as a null hypothesis . This model portrays the pattern of global taxonomic diversification as nothing but a by-product of a myriad of microevolutionary pro­ cesses operating simultaneously upon a vast num­ ber of species in very many environments . Its apparent success, however, may also imply that the empirical pattern of diversity change through geo­ logical time is too heavily loaded by statistical noise to allow identification of the underlying causal process( es) . 4

Mass extinctions. Perhaps the most spectacular debate in modem theoretical palaeobiology con-

553

cerns mass extinctions (Section 2. 12) . When taken in conjunction with the hypothesis that the Cre­ taceous -Tertiary mass extinction was caused by an extraterrestrial impact, the concepts of mass extinc­ tion periodicity (Raup & Sepkoski 1984) and bio­ logical distinctness from background extinction Gablonski 1986) have led to the view that mass extinctions represent a separate class of macro­ evolutionary phenomena, caused by a separate category of macroevolutionary processes. Hence, a general theory of mass extinctions has been sought. Some palaeobiologists have even declared that this new perspective on mass extinctions refutes the neo-Darwinian paradigm of evolution . When con­ sidered in more detail, however, the components of this new perspective do not appear to be demon­ strated beyond any reasonable doubt. The statistical test which was taken to indicate extinction period­ icity seems to be biased toward this result. More­ over, a simple stochastic model is also capable of reproducing the empirical pattern of extinc­ tion peaks through time . Except perhaps for the Permian -Triassic crisis, the individual mass ex­ tinctions turn out to be clusters of events rather than single catastrophes, and there is no evidence to support the claim that they were all due to similar causes . Both hypotheses of an extraterrestrial caus­ ation of the Cretaceous -Tertiary boundary event and of a biological difference between the regimes of mass and background extinction are viable, but other rival hypotheses are at least equally plausible . Thus, any attempt to develop a general theory of mass extinctions must be judged precarious . In terms of its theoretical consequences, the research on mass extinctions may therefore be regarded as fruitless, at least for the moment. On the other hand, it has been enormously productive in terms of empirical data, for it has stimulated much innovative work - palaeontological, microstrati­ graphical, sedimentological, geochemical, and mineralogical - at the stratigraphical horizons con­ sidered to represent times of mass extinction .

Other topics. These four major debates in theoretical palaeobiology of course do not cover the entire area of its research interests . Much consideration has also been given in the last decade to topics such as the evolutionary implications of the ecological or­ ganization of the biosphere . The laws of community evolution have been sought but thus far not found (Section 4. 17), not only because the conceptual framework of community palaeoecology is at pres­ ent too cloudy, but perhaps also because such laws

554

6 Infrastructure of Palaeobiology

are rather unlikely to exist, as ecologists con­ tinue to remind palaeobiologists (Futuyma; Under­ wood; both in Raup & Jablonski 1986) . Van Valen's (1973) Red Queen hypothesis has directed much palaeobiological research toward analysis of the significance of diffuse coevolution for evolution in ecosystems (Section 2 . 5) . Thus far, however, the results are largely inconclusive (Hoffman & Kitchell 1984) . The future

In spite of considerable efforts undertaken within the framework of theoretical palaeobiology, no new biological laws, or even inductive generalizations, have been demonstrated by studies on the history of the biosphere . Perhaps there are no macro­ evolutionary rules which could be detected by palaeobiologists; if so, the nomothetic approach of theoretical palaeobiology would be counterpro­ ductive - but, of course, we cannot possibly know whether or not this is indeed the case . Or perhaps the palaeontological data presently available for palaeobiological analyses are inadequate because they are collected entirely within the framework of palaeontography, for purposes other than testing general hypotheses about the process(es) of evol­ ution . If so, a substantial improvement in the em­ pirical database is badly needed - but such an improvement will only be possible when the gap between theoretical palaeobiology and palaeonto­ graphy is closed. In either instance, however, a change in emphasis for palaeontology appears to be inevitable . Palaeon­ tology has become much more fascinating (and also fashionable) in the last decade than it used to be . It owes this success largely to theoretical palaeo­ biology, because in the eyes of many scientists and public alike the essence of science is to seek general laws . No wonder that palaeontography has often been looked upon as a rather dull, though admit­ tedly necessary, companion of theoretical palaeo­ biology . Yet palaeontology is first and foremost a historical science . Palaeontologists are primarily historians of the biosphere and must focus on re­ constructing history. The history of the biosphere, however, may not be shaped according to a set of general biological laws . Karl Popper's (1945) Poverty of historicism should long have been obligatory read­ ing for palaeontologists . The emphasis of palaeon­ tological research must shift back to the study of unique, historical biological events and chains of events; it must follow the idiographic approach .

Only then should we attempt to seek inductive generalizations about the evolution of lineages, the waxing and waning of clades, mass extinctions and explosive radiations of taxa, etc. Research on particular events and sequences of events, however, should meet the new standards introduced to palaeontology during the last dozen years or so. Models of these phenomena should be developed and rigorously tested, quantitatively whenever possible . To this end, a detailed strati­ graphic framework and a coherent taxonomic system are absolutely crucial. This is not only an empirical challenge but also a theoretical one; for while cladistics may provide a methodology for systematics, its application to taxa of variable geo­ logical age is not a simple matter, and the meth­ odology of biostratigraphy seems to be rather undervalued and consequently underdeveloped. Perhaps even more importantly, however, palae­ ontology must ultimately break down the barriers that have for long separated it from many other disciplines within the earth and life sciences. In the last decade, these barriers have already begun to collapse . On the one hand, palaeontologists are beginning to look to molecular and cell biology for a better understanding of fossil organisms (Section 2 . 1 ) . This may lead to the demonstration that mor­ phogenesis of the skeletal parts - which are the objects of palaeontological study - is under much stronger environmental controls than traditionally accepted . Were it so, the implications for palaeon­ tological interpretation of fossil morphologies and their variation in space and time would be tremen­ dous. On the other hand, palaeontologists are beginning to view the biosphere as a component of a global system which encompasses life, ocean, air, and the lithosphere . This trend is reflected by the growing interest among palaeontologists in stable isotope geochemistry, palaeoceanography, and palaeoclimatology (Section 4. 19) . The promise of these disciplines for the history of the biosphere lies in their potential to shed new light on the workings of the global system and hence, indirectly, on the state of the biosphere . For the future of palaeontology, I thus envisage a more humble focus on reconstruction of the history of life, rather than on attempts to discover the laws of this history; but I also envisage a considerable expansion of the scope of palaeontology to include all aspects of the history of life on Earth, rather than solely the history of particular lineages, clades, or communities . To this end, however, we must always be very explicit about the biological entities we

6.5

History of Palaeontology

undertake to describe and reconstruct - whether we talk of genotypes, phenotypes, or single traits, whether of phena, biological species, or phyletic lineages, whether of taphocoenoses, ecological com­ munities, or taxocoenoses - and we must also be explicit about the limitations of our biological inter­ pretations . Otherwise, palaeontology will inevitably fall back to the stage of mere story-telling. References Brinkmann, R. 1929 . Statistisch-biostratigraphische Unter­ suchungen an mitteljurassischen Ammoniten uber Artbegriff und Stammesentwicklung . Abhandlungen der wissenschaftlichen Gesellschaft zu Gottingen 13(3), 1 - 249 . Hoffman, A. 1988 . Arguments on evolution: a paleontologist's perspective. Oxford University Press, New York. Hoffman, A. & KitcheII, J.A. 1984. Evolution in a pelagic planktic system: a paleobiologic test of models of multi­ species evolution. Paleobiology 10, 9-33.

555

Jablonski, D . 1986 . Background and mass extinctions : the alternation of macroevolutionary regimes. Science 231, 129 - 133 . Popper, K . R . 1945 (book edition i n 1960) . The poverty of historicism. RoutIedge & Kegan Paul, London . Raup, D.M. & Jablonski, D. (eds) 1986 . Patterns and processes in the history of life. Springer-Verlag, Berlin. Raup, D.M. & Sepkoski, J.J., Jr. 1984. Periodicity of extinctions in the geologic past. Proceedings of the National Academy of Sciences of the United States of America 81, 801 - 805 . Schopf, T.J.M. (ed . ) 1972 . Models in paleobiology. Freeman, Cooper and Co. , San Francisco. Sepkoski, J.J. Jr. , 1978. A kinetic model of Phanerozoic taxo­ nomic diversity. I. Analysis of marine orders . Paleobiology 4, 223-251 . Stanley, S.M. 1975 . A theory of evolution above the species level . Proceedings of the National Academy of Sciences of the United States of America 72, 646 -650. Van Valen, L . 1973 . A new evolutionary law . Evolutionary Theory I, 1 -30.

Index

Note : numbers shown in italic type refer to illustrations, and those shown in bold type refer to tables.

abiotic soils, 57, 58 abrasion destructive process, 223, 224, 224, 225, 225, 233, 237 taphofacies, 258, 258, 259, 260, 262, 263 abrasive techniques, preparation, 500

Acanthina, 368 acanthocephalans, parasites, 377 acanthodian fish, extinction, 185

Acanthorhina, 284 Acanthostega, 69 Acanthoteuthis, 287 Acarina, Baltic amber, 297, 297 acceleration, heterochrony, 1 1 1 , 1 1 3, 1 1 3 , 1 14, 1 1 7 acceleration forces, hydrodynamics, 323, 324, 324, 325 acetic acid, sample preparation, 501 , 501 ,

502, 503 Acheulean, 89- 90 acid rain, 163, 165 acids, sample preparation, 501 , 501 , 502,

aclonal organisms, 43, 47, 331 acme biozone, stratigraphy, 461, 467, 467 acritarchs Hunsriick Slate, 279 Palaeozoic, 51 , 52, 182, 1 83 Precambrian, 1 1 , 15, 1 7, 50, 1 79 - 80 problematic taxa, 443 stratigraphy, 461, 478 thermal maturity, 513, 514, 5 1 4 actinopterygians biogeography, 449, 450, 450, 451 extinction, 189, 192 feeding, 366 Adapoidea, stratophenetics, 440, 441 adaption, 139 - 46 'adaptationist programme', 143 'adaptive gaps' , coevolution, 137 'adaptive peaks', selection, 128 'adaptive value', 140 experimental morphology, 308 - 9 predation, 368 radiations, 127 Adaptiver Aspekt, morphology, 3 1 1 adhesives, sample preparation, 501 -2 Aegyptopithecus-like, 440, 441 Aepycerotini, lineages, 128 aerobic environment decay, 213- 14, 216, 223 diagenesis, 251, 252 fossil indicators, 409, 4 1 0 Precambrian, 13- 14, 1 4 , 16 source rocks, 221 taphofacies, 259, 259, 260, 261 , 262, 263

503

aerodynamics, flight, 75, 7 6 aetosaurs, predators, 373 agamids, 205, 206 Agaricia, 343 Agerostrea mesenterica, 142, 1 42 aggregation colonies, 331 encrusters, 350

Aglaophyton major, 62 agnathans feeding, 366 Hunsriick Slate, 279 Agnostus pisijormis, 2 75, 276 agrichnia, trace fossils, 356 Agricola, G . , (1494- 1555), 537 Ain Deliouine, Morocco, 481 - 2 air embolism, trees, climate indicator, 402

Akidograptus ascensus 480 akinetes, Precambrian, 13 207 alanine, brachiopods, 98 Albertosaurus, 205, 207 Albumares, 18, 1 9 Alcelaphini, lineages, 128 n-alcohols, organic components, 219 alcyonarian octocorals, 26, 4 5 , 48

Alamosau rus, 205,

Aldanella, 34 Aldrovandi, U . , (1522 - 1605), 537- 8 alete spores, 60 algae brown, 30 destruction of, 224 diagenesis, 247, 248, 250 encrusters, 346, 349 endolithic, 224, 248 environmental indicators, 406, 4 1 1 , 412 Hunsriick Slate, 279 mats, 336 Ordovician, 54- 5 prasinophyte, 1 5 , 50, 5 1 Precambrian - Cambrian, 1 4 , 1 5, 29, 30, 50, 5 1 , 53 problematic taxa, 443 prymnesiophyte, 220 receptaculitid, 54, 443 reefs, 341, 342, 342, 345 skeletons, 316, 3 1 6 source rocks, 220 terrestrialization of, 60, 6 1 Vendotaenian, 17, 180 see also green algae; red algae alkalinity, ocean, 1 63, 165 alkanes, source rocks, 219 n-alkanones, organic components, 219 Alken fauna, Germany, 68 alkenones, source rocks, 219, 220 alleles, 100, 101, 102, 103, 104, 327 allometry, 1 1 1 allopatric speciation, 104, 105, 107, 448 allozymes, populations, 327- 9, 327, 328,

Allosaurus, 363, 374

557

329, 329

231 Alpha diversity, 1 33, 134, 134 Alpine belt, biostratigraphy, 484 Alum Shale, Sweden, 274- 7, 2 75 Alvarez hypothesis, extinction, 167 amber, Baltic, 294- 7, 294, 295, 296, 297

Alnus glutinosa,

Ambitisporites, 62, 64 amino acids origin of life, 3, 4, 5, 7 sequences, 1 7, 31, 95, 97-8, 98, 99, 100 source rocks, 217 ammonia, taphonomy, 241, 252, 292 ammonites adaption, 143 baculitid, 1 14 extinction, 1 60, 1 66, 1 67, 1 72 Cretaceous - Tertiary, 202, 400 end-Permian, 189, 191, 1 92 end-Triassic, 194, 1 95, 196, 1 96 biogeography, 457, 458 biomechanics, 320, 321 biostratigraphy, 461, 462, 463, 465, 466,

467, 484 environmental indicators, 412 feeding, 364 goniatitic, 189, 484 heterochrony, 1 14, 1 15, 1 1 7 lineages, 428 Lagerstatten, 267, 268, 270, 283, 284 Solnhofen Limestone, 285, 286, 287,

288 phragmocone, 244, 244, 245 speciation, 108 taphonomy, 244, 244, 245, 251 , 252, 259 ammonium chloride, photography, 505 amniotes classification, 435 -6, 436 terrestrialization, 68, 69, 70 amoebae, parasitic, 380 amorphous organic material (A . O .M), vitrinite reflectance, 512, 514 amphibians branchiosaurid, 1 14, 1 1 5 evolutionary faunas, 39, 41 extinction, 189, 190, 1 90, 194 heterochrony, 1 14, 1 1 5, 1 1 7 - 8 morphology, 3 1 2 , 3 1 3 predators, 373, 376 temnospondyl, 70 terrestrialization, 69, 70, 71 amphicyonids, predators, 375 amphipods, terrestrialization, 66, 67, 68

Amphipora, 56 Amplexopora, 351 Anabarites, 44 anabaritids, 24, 25 Precambrian - Cambrian, 34

Anadara mon tereyana, 409 anaerobic environment decay, 213, 214, 223

558

Index

diagenesis, 251 - 2, 252, 253, 254, 255 fossil indicators, 409, 4 1 0 LagersUitten, 270, 283 Precambrian, 7, 12, 1 3 - 14, 14, 16 source rocks, 221 taphofacies, 259, 260, 261 anagenesis, 106, 107, 109, 1 15, 126 computer analysis, 498 Anahuac Formation, Texas, 41 1 , 412 anamniotes, compared to amniotes, 70 anaspids, evolutionary faunas, 39, 41

Alwtolepis, 27 Anceps Bands, Dob' s Linn, Scotland, 479,

480

Al1clzitlzeriunr, 86 Al1coricl1l1us, trace fossils, Al1festa stalzkovskii, 18, 20

358

Angaran flora, 191 angiosperms climate indicators, 401 , 402 evolution, 39, 40, 67, 79 -83, 80, 81 , 82, 83, 85, 101, 102, 354 processes of, 133, 1 35, 138, 147, 148 hydrodynamics, 232 nomenclature, 422 preservation, 264 resin, 295 anguidae 205, 206 ankylosaurs defence, 375 feeding, 363

Al1kylosaurus, 375 ankylosis, palaeopathology, 382 annelid worms feeding, 364, 388 LagersUitten, 240, 276, 277, 2 78, 288 parasitic, 378 Precambrian - Cambrian, 18, 21, 25 size constraints, 149 terrestrialization, 64, 65 trace fossils, 360

Al1onzalocaris cal1adensis, 215 Anomalodesmata, predation, 389, 390 anoxic environment Cambrian, 36 decay processes, 214, 223 extinction, 161, 1 62, 163, 189, 198 indicator fossils, 409, 4 1 0 Lagerstatten, 239, 241 , 267, 268, 290 - 1 taphofacies, 259, 259, 2 6 1 , 262, 263

Anoxiunr, 49, 50

anteosaurs, predation, 373 anthoecia, grasses, 84 anthophyte, clade, 79, 80, 81 , 82 anthozoans see corals antibodies, molecular fossils, 98 - 9 Anticosti Island, Canada, 182, 479 antilocaprids, 87 antimony oxide, photography, 505

An tiquilinra, 283 An trinrpos, 287 apatite skeletons, 24, 27, 256, 256, 257, 314,

316

Apatosaurus, 319, 382 apical angle, shells, 227, 229 Apidiun r -like, 440, 441 aplacophorans, trace fossils of, 360

Apollon nalalor, 390 Appalachians, 184, 185, 1 86, 396, 396 'aptations' , 145 apterygote insects, 65, 72, 73, 74 Baltic amber, 297, 297 Aptian, extinction, 1 74, 1 75

aptychi, Lagerstatten, 286 arachnids Baltic amber, 297, 297 coevolution, 137 terrestrialization, 59, 65, 66, 67, 68 trigonotarbid, 59, 65 aragonite diagenesis, 247, 248-9, 248, 249, 250, 256 durability, 225 environmental indicators, 403, 408 precipitation, 35, 36 Lagerstatten, 267, 283, 288 skeletons, origin of, 24, 25, 25, 26, 28, 201 , 314, 315, 3 1 5 , 316, 3 1 6, 317 Araneae, Baltic amber, 297, 2 9 7 arborescent, skeletal type, 225, 226 Archaean, 1 0 - 13, 1 1 , 13, 14, 1 6 stratigraphy, 4 7 1 , 474 stromatolites, 336, 338 - 9, 338 Arclzaeantlzus, 82, 82 archaebacteria Precambrian, 7, 12, 16 taphonomy, 219, 292 archaeocyathids hydrodynamics, 325 Precambrian -Cambrian, 22, 23, 25, 26, 44, 45, 45, 53, 54 problematic taxa, 442 reefs, 342 archaeogastropods extinction, 193 predation, 371

Archaeoleersia, 84 Archaeopteris, 422 Archaeopteryx, 375, 427, 543 flight, 76, 78 Lagerstatten, 270, 287, 288, 289, 543

Arc/zaeopteryx lithographica, 125 Archaeoscyplzia, 54 Arc/zaeosphaeroides, 50, 51 Archinredes internridius, 325 Architectonica nobilis, 455 archosaurs classification, 436 extinction, 190, 1 90, 194, 195, 1 95 flight, 76, 78 predators, 373, 374, 374 see also pterosaurs arctocyonids, predators, 375 Arctodus, 208, 208 Arenicolites, 359 aridity, extinction, 197 Arizona fossil forest, 264, 266 armadillos, extinction, 208, 208

Arnioceras, 364 Arpylorus, 50 Arthropleura arnrata, 364 arthropleurids, 65 arthropods biomechanics, 318, 319, 320, 320, 321 , 322 Cambrian, 33, 44 coevolution, 137-8 environmental indicators, 406 extinction, 187, 189 feeding, 362, 364, 365 -6, 370, 388 flight, 72-5, 73 heterochrony, 116, 1 18 Lagerstatten, 268, 269, 271, 2 72 , 281 , 286, 286 Hunsruck Slate, 277, 278, 279 'Orsten' deposits, 274, 2 75, 276 - 7 moulting, 26, 68, 149, 3 1 7, 319 parasitic, 377 - 8, 3 77

phyllocarids, 370 plants, and, 354 podomere, 319, 320 Precambrian, 18, 21, 22, 27, 34 predators, and prey, 370, 3 7 1 , 373 resin trapped, 296, 296 size constraints, 149 taphonomy, 223, 245, 246, 257 terrestrialization, 41, 64, 65, 66, 67-8 see also arachnids; chelicerates; crustaceans; insects; ostracods; trilobites articulate brachiopods environmental indicators, 406 extinction, 189, 192, 193 Palaeozoic fauna, 38 articulation, taphonomy, 223, 225, 226, 237 taphofacies, 258, 258, 259, 260 - 1 , 260, 262, 263 Lagerstatten, 277, 286, 291 artificial intelligence programming, 498 Asaphocrinus ornatus, 240

Ascarina, 79, 82 ascidians, encrusters, 350 ascomycetes, terrestrialization, 58, 59, 63 ascothoracicans, parasites, 378 Ashgillian extinction, 37, 40, 181 aspartic acid, effect on skeletons, 317

Aspidoceras, 287 asses, evolution, 86 assemblages biozone, stratigraphy, 461, 467, 467 communities, 237- 8, 238, 391 association, communities, 391 Asteriaci tes, 359 asteroids extinction process, 1 64, 1 65, 1 67, 203 Lagerstatten, 268 predation, 370 astogenetic heterochrony, 1 1 7 astogeny, colonies, 330 astrapotheres, size, 150 atmosphere, origin of life, 8 - 9 atolls, 56 atrypid brachiopods, biofacies, 399 Atrypoidea, extinction, 400 attitude, shells, 226, 227 -8, 229, 239, 258, 259 260, 262, 281 Auchenorrhyncha, in amber, 297

Aulichnites, 359 Aulopora, 348 aurochs, size, 150

Ausia, 21 Australopithecus afarensis, 88,

89 autapomorphies, 431 , 431 , 432 autochronology, 473 autochthonous deposits amber, 294, 295 Solnhofen Limestone, 288 autocorrelation analysis, extinction data,

1 74, 1 76 autoregressive models, extinction, 1 76 autotrophic evolution, origin of life, 6, 7,

'avatars' , 126, 126 A ves see birds Avogadro's Principle, 213

8, 12

Aysheaia, 65 Backlundtoppen Formation, Spitsbergen, 11 backwards-smearing, of stratigraphic

559

Index ranges, 1 66 bacteria decay, 213- 16, 2 1 5 , 2 1 6 green, 49 infection, 382 -3, 384 molecular evidence, 96 Precambrian, 7, 17, 49, 50 stromatolites, 336 taphonomy, 220, 223, 253, 254, 256 Lagerstatten, 268, 273, 281, 282, 288,

292 - 3 baculitid ammonites, heterochrony, 1 1 4 11 Bahama Banks, compared Archaean, . Bajocian extinction, 167 Bala unconformity, Wales, 483 Baltic amber, 294- 7, 294, 295, 296, 297 Baltic Sea, salinity, species diversity, 407, 407 Baltica, biostratigraphy, 485, 487 Baltoeurypterus, 321, 322 banded iron formations, 49 Baragwanathia 61 , 62, 64 barium sulphate, Burgess Shale, 273, 274 barnacles, encrusters, 346, 347, 348, 350 barrier reefs, 56 Baryonyx, 363, 375, 501 basaltic volcanism, 1 70, 178 basidiomycete fungi, terrestrialization, 59

Basilosaurus, 148, 151

bathymetry extinction, 184 - 5 trace fossils, 360

BathY11lodiolus ther11lophilus, 390 bats feeding, 365 flight, 75, 76, 77, 78 Lagerstatten, 241 , 292 Bautechnischer Aspekt, morphology, 3 1 1

Bavarisaurus, 363 Bavlinella faveolata, 1 79 - 80 beam theory, biomechanics, 319, 320 bears extinction, 208, 208 feeding, 367 palaeopathology, 382, 382 Beaufort Series, South Africa, 190 - 1 Beck Springs Dolomite, California, 5 1 , 53 beetles, predators, 373 behavioural classification, trace fossils, 355 - 6, 355 Belcher Supergroup, Hudson Bay, Canada, 13, 5 1 belemnites extinction, 400 geochronology, 483 oxygen isotope ratios, 403 taphonomy, 227, 228, 229, 247, 252 Lagerstatten, 283, 284, 284, 286, 288 Bennettitales, Cretaceous, 80, 81, 8 1 benthic environment biofacies, 396- 7, 397 Lagerstatten, 283, 284, 284, 286, 288 microevolution, 1 08, 1 10 bentonites, stratigraphy, 465 Bermuda lagoonal patch reef, 343, 345 Bernal' s clay theory, 5, 8 Bernoulli equation, 323, 325

Berriochloa, 84 bicarbonate ion, diagenesis, 251, 252

Bija, 26 Bilateria, Precambrian, 18, 2 1 - 2 Binominal Nomenclature, Principle of,

417, 422 - 3

biochronology, 464, 465 biocoenoses, 258 biodepositional structures, trace fossils, 355 bioerosion skeletons, 223, 224- 5, 237, 258 structures, trace fossils, 355 biofabric fossil concentration, 235 - 6, 236, 237, 258 shells, 227- 8, 228, 229 biofacies, 391 , 395- 400, 395, 396, 397, 399 oxygen indicators, 409, 4 1 0 tectonics, 485 -6, 487 'Biogenetic Law', 1 1 1 biogeography palaeobiogeography, 452 - 60, 452, 453, 454, 455, 456, 457, 458, 459 vicariance, 448 - 5 1 , 450, 451 bioherms, 53, 54, 55, 184 biohopanoids, molecular fossil, 95, 96 bioimmuration, encrusters, 346 biological marker, 2 1 7, 218-20, 292 biomass increase due to new habitats, 120 trophic structures, 388, 388, 389 biomechanics, 318-22, 3 1 9 , 320, 322 biomineralization see mineralization biominerals, organic compounds, 97-9, 98 biopolymers, diagenesis, 217 biostratigraphy, 461 - 5, 4 6 3 , 464, 549 International Commission on Stratigraphy, 468- 9 International Geological Correlation Programme, 469- 70 trace fossils, 355, 357 zone fossils, 466- 7, 466, 467 see also global standard stratigraphy biostromes, 53, 54, 55, 343 biotaxonomic classification, trace fossils,

424 - 5 bioturbation evidence from, 43, 45, 389 palaeosols, 58 Precambrian - Cambrian, 23, 31 structures, trace fossils, 355 taphonomy, 221, 225, 283 - 4, 291 biozones, 461 , 462, 463, 463, 464, 466, 467 compared to biofacies, 395 bipeds archosaurs, 76 hominids, 88 birds biomechanics, 319, 321 classification, 436, 436 diversity of species, 132, 1 3 2 evolutionary faunas, 39, 41 extinction, 207 flight, 75, 76, 77, 78 heterochrony, 1 14 Lagerstatten, 241 , 292 predators, 368, 375, 376 skeleton, 314 speciation, 105 Birkhill Shale, Dob's Linn, Scotland, 479,

480 bison, 55 bisporangiate condition, coevolution, 138 Bitter Springs Formation, Australia, 1 1 , 51 ,

53 bituminous deposits, Lagerstatten, 270, 282, 283, 283, 286, 290 bivalves biofacies, 396, 397, 398, 399, 399, 400

biogeography, 454, 455, 456, 457, 459, 460 conchiolin, 223 destruction, 223, 224, 225, 226 diagenesis, 249, 250 diversification, 38, 46, 47, 48, 52 encrusters, 346, 347, 349 environmental indicators, 403, 404-5, 405, 406, 409 extinction, 184, 187, 189, 191, 192, 194,

195, 201 -2, 400 feeding, 363, 389- 90, 390 fossil concentrations, 236 heterochrony, 1 15 heterodont, 400 immunological techniques, 99 inoceramid, 201, 400 Lagerstatten, 242, 243, 267, 270, 279, 281 ,

283 -4 lucinid, 390 nuculid, 224 parasites of, 380 pearls, 378 - 9 preadaptive hypothesis, 144, 1 45 prey, 368, 369, 370, 371 reefs, 341, 342, 342, 343 size, 151 solemyid, 390 speciation, 108 stratigraphy, 465 survivorship curves, 1 20, 1 22, 124 thyasirid, 390 transport, 227, 228, 229 trophic structure, 389 - 90 see also rudist bivalves Black Sea, 221 black shales extinction, correlation with, 161, 1 82 obrution deposits, 239 blastoids completeness of record, 301 Palaeozoic, 46, 47, 89 Blind River Formation, Ontario, 57 bloodsucking parasites, 376 ' blue earth' , Baltic amber, 294, 294 blue-green algae, see cyanobacteria, stromatolites Bodo, Ethiopia, 90 Bog people, Iron Age, 213, 214 'Bohemian' sediments, 277 boids, record of, 205, 206 bolides, extinction process, 165 B011lakellia kelleri, 20 Bomakellidae, Precambrian, 20, 21, 21 - 2 bone beds, concentration deposits, 267 bones diagenesis, 254, 255 fracture healing, 381 - 2, 384 transport - hydrodynamics, 232- 5, 234 book-lungs, terrestrialization, 67 bootstrapping, computer analYSis, 495 Bopyridae, parasites, 378 boreal forest, Pleistocene, 84 borers, effect on reefs, 54, 55, 56 Borhyenidae, predators, 151

Bositra, 284 botryococcanes and botryococcenes, biomarkers, 219

Botryococcus braunii, 219 Boundary Stratotype Point see Global Stratotype Section and Point (GSSP) bovids, Tertiary, 87 Bowen Basin, Australia, 265 Braarudosphaera, 201, 316, 3 1 6

560

Index

brachiopods amino acid profiles, 98 atrypid, 399 biofacies, 396, 398, 399, 400 biostratigraphy, 480, 481, 485, 486 Cambrian, 23, 24, 25, 34, 44, 45 origin of hard parts, 27, 28, 29 community evolution, 392 completeness of fossil record, 302 coquinas, 267, 269 craniacean, 1 14 destruction of, 223, 224, 225, 226 diagenesis, 247, 248, 249, 250, 255 encrusters, 346, 347, 349 environmental indicators, 403, 405, 405,

406, 409, 4 1 1 , 412 extinction Cretaceous - Tertiary, 1 60, 200, 202 Frasnian - Famennian, 184, 186 Ordovician, 181, 1 8 1 , 182, 1 83 Permian, 187, 187, 189, 191, 193 Triassic, 192, 194, 195 flattening, 245, 246 geochronology, 483 heterochrony, 1 14, 1 15, 1 1 6 hydrodynamics, 227, 229 inarticulate, 192, 433 Lagerstatten, 240, 272, 273, 273, 276, 277,

279 lineages, 428 modern, 48 orthid, 189, 398, 399 Palaeozoic, 38, 40, 45, 46, 47, 52, 54, 55,

480 parasites of, 380 pentamerid, 399, 400 prey, 369, 370, 371, 3 71 , 372 productid, 1 60, 189, 400 rhyonchonellid, 400 size constraints, 149 - 50 skeleton, 318 strophomenid, 194, 399 taxonomy, 433 terabratulid, 400 thecideidine, 1 1 4 Vendian, 22 see also articulate brachiopods Brachiosaurus, 147, 148, 149 brachyuran crabs, predation, 370 bradoriids, biomineralization, 25, 27 'bradytely' , 153, 1 58 - 9, 158 Braggs River, U . 5 . A . , 201 Braidwood biota, 279, 281 brain size, hominids, 88, 89, 90, 91 branchiosaurid amphibians, heterochrony, 1 14, 1 1 5 Brazons River, U . 5 . A . , 201

Bredocaris admirabilis, 276 breeding time, reproductive isolation, 101 brittle stars, preservation, 240, 242, 243,

268, 283 bromoform, concentration techniques, 504 Brongniart, Adolphe, (1801 - 1876), 540 - 1 ,

542 Brongniart, Alexandre, (1770 - 1847), 540 Bronn, H . G . , 545 brontosaurs, predation, 375

Brooksella canyonensis, 30 brown algae, diversification, 30 browsers grasslands, 85, 86 trophic structure, 385, 386, 388

bryophytes, terrestrialization, 58 -9, 58,

60, 62, 63 bryozoans biofacies, 398, 399 biomineralization, 25 coloniality, 330, 332, 332, 333, 334 cryptostomate, 160, 189 diversification, 40, 46, 47, 48, 54, 55 encrusters, 346, 348, 349, 350, 351 environmental indicators, 411 extinction, 1 60, 187, 187, 189, 192, 201,

202

gymnolaemate, 40, 48 heterochrony, 1 1 7 hydrodynamics, 325, 325 parasites of, 379 reefs, 342, 342, 343, 345 size constraints, 149 speciation, 1 08 stenolaemate, 38, 46, 347 taphonomy, 224, 247, 248, 279 trepostome, 160, 189 Buckland, W., (1784 - 1856), 542, 542 Buffon, G . L . Compte de ( 1 707 - 1 788), 539

Bugula turrita, 325 build-ups, 53, 54, 55, 56, 341 - 5, 342, 343, 344 Bundenbach district, West Germany, 254 buoyancy, biomechanics, 49 - 50, 320 Burgess Shale, British Columbia, 52, 215, 239, 269, 270 - 4, 2 72 , 2 73 , 398, 426,

548 - 9 dietary evidence, 362, 364 flattening, 245, 246, 246 Hunsrtick Slate compared, 278 parasites, 377 terrestrialization, 65 tiering structure, 45 Burgess Shale-type assemblages, 33, 34

Burgessochaeta, 364 burial obrution deposits, 239- 43, 240, 241 , 242 plant material, 232 skeletons, 226, 235 Burin Peninsula, Newfoundland, Canada, 476, 477 burrowers Cambrian, 29, 31 destructive processes, 223 Precambrian, 22, 23, 180 reefs, effect on, 54 see also infauna

Busycon, 368 'Bynes Disease' , fossil storage, 516

durability, 201 , 225 Lagerstatten, 267, 283 Precambrian - Cambrian, 24, 25, 26,

28, 29, 35, 36 size, 150 calcium binding proteins, 99 salinity indicator, 407 calcium carbonate concretion, 259 plant preservation, 264 skeletons, 247- 50, 248, 249, 256 Precambrian- Cambrian, 24, 25, 25,

26, 29, 34 stromatolites, 337- 338, 339- 40 supersaturation, 15 see also aragonite; calcite calcium phosphate coprolites, 366 polymorphs, 36 skeletons, 25, 27, 34, 254, 317 Caledonian mountain belt, 485 Calippus, 86, 87

Callianasa, 364 Callixylon, 422 callus, bone, 382

Calytogena magnifica, 389- 90 Cambrian biofacies, 396, 398 communities, 393 decay process, 215 diversification, 34- 6, 35, 132, 133 marine habitats, 45, 45, 46, 47, 47, 50-2, 51, 53, 54 evolutionary faunas, 37, 38, 38, 39- 40, 39 extinction, 160, 1 79 - 80, 1 80 global boundary stratotypes, 475 - 8, 477 heterochrony, 1 17, 1 1 8 morphology, 309 parasites, 378, 379 predation, 370, 371 problematic fossils, 442, 443, 444 skeletal composition, 318 stratigraphy, 461 , 470, 475- 8, 4 7 7 , 486 stromatolites, 336, 337, 339, 340 terrestrialization, 57-8, 58, 59, 65 trace fossils, 360 Vendian compared, 23 see also Burgess Shale; ' Orsten' cambroclaves, Cambrian, 25, 34 camels decline, 208, 208 dentition, 86

Camenella, 27 Cache Creek Terrane, British Columbia,

487

Calamites, 1 5 1 , 245 Calappa, 369 Ca/athium, 54 calcareous rocks, extraction techniques, 502, 503 Calceolari, F., (c. 1 521 - c . 1606), 538 calcic horizons, grassland soils, 85 calcite destruction of, 225 oxygen isotope ratios, 403 plant preservation, 263, 264, 281 skeletons, 314, 315- 16, 3 1 5 , 3 1 6, 317, 318 diagenesis, 245, 247, 248 -9, 248, 249,

250, 251, 252, 256

camerate crinoid, extinction, 160, 1 89 Canada, legislation concerning status material, 517 Cancellariidae, parasites, 390 cancer, palaeopathology, 382 cannibalism, 364 Canning Basin, Western Australia, 56, 345 carbohydrates, decay, 217 carbon, organic biogeochemical cycle, 120 decay processes, 213, 214 Precambrian, 49 source rocks, 220, 221 carbon dioxide, 292, 293 decay product, 213 diagenesis, 251, 252 extinction process, 164, 165, 1 78

561

Index Precambrian- Cambrian, 12, 36 terrestrialization, 57 carbon isotopes decay processes, 216 extinction processes, 167 Precambrian - Cambrian, 12, 35, 35, 36,

49, 58 carbonate-fluorapatite, 256, 257 carbonates biofacies, 398, 399- 400 extinction events, 181, 182, 183, 1 84, 199 molecular palaeontology, 97 mounds, 341 nodules, 240 - 1 , 250 -2, 251 , 252 skeletal fossils, 24- 7, 25, 28, 28, 29, 314,

315 salinity indicator, 407 stromatolites, effect on, 337- 8 see also aragonite; calcite; calcium carbonate Carbondale Formation, Illinois, 279 carbonic acid, diagenesis, 251 Carboniferous, 40 adaption, 142 biomechanics, 319 coevolution, 137 decay process, 214, 2 1 5 dietary evidence, 364, 365 diversification, 40, 47, 1 32 environmental indicators, 405, 405, 408,

41 1 , 412 Lagerstatten, 239, 297 nomenclature, 422, 423 parasites, 377 plant communities, 352, 354 preservation, 264, 265 predation, 371, 373 reefs, 344 size, 150, 151 terrestrialization, 58, 59, 65, 67, 71, 71, 72 see also Mazon Creek Carcharodon, 148, 149, 363 Carnian, extinction, 174, 1 75 Carnic Alps, Italy, Devonian, 277 carnivores bone transport, 233 coevolution, 137 coprolites, 366 evolution rate, 153 extinction, 193 feeding, 362 land vertebrates, 373, 374-5 size, 150 carnosaurs, feeding, 363, 374 carpel, angiosperms, 80, 82 Carpolestidae, stratophenetics, 439, 439 carpometacarpus, birds, 78 caryopses, grasses, 84 cassid gastropods, predation, 370 cat, predators, 375 - 6 catabolic processes, 8 catastrophism extinction process, 171 Lagerstatten, 271

Catinula, 108 cation concentration, Precambrian, 31

Caturus, 364 caves dietary evidence, 367 hominids, 90, 91 caviomorph rodents, extinction, 208

Caytonia, 80, 8 1 Ceboidea, stratophenetics, 440, 441 cells eukaryotes and prokaryotes, 30 plant preservation, 264, 264, 266 cellular control, heterogeny, 1 18 cellularity, origin of life, 3, 4 cellulose decay, 214, 2 1 5 diagenesis, 254 digestion, 85, 87 cementation, Solnhofen Limestone, 287 cemented forms, encrusters, 346 Cenomanian extinction, 167, 1 70, 1 73 , 1 74, 1 75, 176, 1 77 Cenozoic biogeography, 456, 457 coevolution, 136, 137, 138 communities, 391 diagenesis, 250 dietary evidence, 367 diversification, 40, 48, 1 32 encrusters, 347, 349 environmental indicators, 404, 404, 405, 406, 408 heterochrony, 115 microevolution, 109 molecular palaeontology, 97 parasites, 377 - 8 predation, 370, 372, 373, 376 stratophenetics, 439, 440, 441 stromatolites, 336, 340, 340 taxonomy, 447 trophic structure, 386, 387 centipedes Lagerstatten, 279 terrestrialization, 65

Cepaea nemoralis, 140, 141, 143 cephalon, taphofacies, 259 cephalopods biomechanics, 320, 321 ceratitid, 194 environmental indicator, 406 extinction, 187, 191, 194 feeding, 362, 363 hydrostatics, 322 Lagerstatten, 254, 279, 281, 288 Palaeozoic, 38, 40, 46, 52, 54 predators, 368, 369, 370 prey, 372 rhyncholites, 370 shell, transport, 227 see also ammonites, belemnites

Cerastoderma, 228 ceratitid cephalopods, extinction, 194 ceratopsian dinosaurs defence, 375 extinction, 205, 207 feeding, 364 Ceratosau rus, 374 cerberoid colonies, 333 Cercopithecoidea, stratophenetics, 440,

441 cerium phosphate, Burgess Shale, 2 73 , 274 cervids, diversity, 208 cestodes, parasites, 377 Cetacea evolution rates, 15 size, 148 chaetognaths Cambrian, 28, 34 marine habitat, 64

chalk production, Cretaceous, 201 , 202 Chambers, R . , 545 chamosite, taphofacies, 259 chancelloriids, Cambrian, 34 chaotic behaviour, computer modelling,

296, 297 charge free anticontamination system (CFAS), 509, 5 1 1 Charnia, 1 9, 20, 21, 180 Charnian Subgroup, U.K., 1 7

Charniodiscus, 21, 44, 180 Charophyceae, terrestrialization, 63 Charnwood Forest, U.K., 32 chartaceous leaves, hydrodynamics, 231 cheilostomes, encrusters, 347 chelating agents, sample preparation,

500 - 1 chelicerates biomechanics, 320, 320 Lagerstatten, 276 terrestrialization, 67, 68

Cheloniellon, 278 Cheloniidae, 205, 206 chemautotrophic bacteria, 49, 51 chemical fossils, 217-22, 2 1 8 , 2 2 1 chemostratigraphy, 469, 471, 472, 478 cherts, extraction techniques, 503- 4 chirality, coccoliths, 3 1 6 Chiroptera, flight, 78 chitin, preservation, 214, 2 1 5, 276

Chitinobelus, 284 Chitinozoan Reflectivity (Rch), 5 1 3 chitinozoans biostratigraphy, 461 diversity, 51 , 52 extinction, 182 parasites of, 380 problematic taxa, 443 -4 sample preparation, 502, 504 thermal maturity, 5 1 3 , 513, 514 chitons, Lagerstatten, 279, 281 Chloranthaceae, evolution, 79, 80, 81, 82

Chloranthu5, 82 Chloroflexus, 7 chlorophycid, Proterozoic, 50, 5 1 chlorophyll A , breakdown, 96, 97 chlorophytes, terrestrialization, 57 choana, tetrapods, 69 Choia, 2 73 cholesterol, zooplankton, 217, 2 1 8 chondrichthyan fishes feeding, 366 Palaeozoic, 38, 40 size, 148 Chondrites, 283, 359 chondrophorans, Vendian, 32, 50

Chondroplon, 18 Chondrostei, extinction, 189, 192

Chondrosteus, 284 chordates biomineralization, 27 Burgess Shale, 2 72 chromatographic techniques, 96 chromosomes, reproductive isolation,

101 -2 chronostratigraphy, 462 - 5, 463 , 464, 468,

471, 472, 474 chronozones, 461, 463, 464 chroococcaleans, Precambrian, 50, 180 chrysophytes, Cambrian, 25, 28, 50 Chuar Group, Arizona, 1 1 cichlid fish, experimental morphology, 308

562 ciliates, parasitic, 380 cirripedes encrusters, 346, 347, 348, 350 parasites, 378 clade, 1 34 - 5, 436 cladistics, 426 - 7, 428 - 30, 430 - 4, 43 1 , 435, 436, 437 angiosperms, 80 - 1 biogeography, 449 - 50, 450, 451 , 452 - 3 , 452 , 454, 455 computer analysis, 497 diversity, 448 fossil record, 299 future of, 551, 554 morphology, 3 1 3 stratophenetics, compared, 438, 441 see also cladogenesis cladogenesis, 1 06, 107, 1 08, 1 09, 126, 138 community, 394 computer analysis, 498 evolution rates, 1 54, 1 58, 1 58 heterochrony, 1 15 parasites, 377 cladograms, 433 - 4 Claria, 1 9 1 Classes, evolutionary faunas, 3 7 classifica tion definition of, 434 evolutionary systematics, 435 - 6 nomenclature, 422 - 3 Clavatipol/enites, 79, 80, 82 clay deposition, extinction events, 1 67, 1 69, 1 69, 202 clay minerals, origin of life, 5, 6 Climacograptus extraordinarius, 1 8 1 , 478, 479 climate biostratigraphy, 461 effect on diversification, 1 33 - 4 factor i n extinction, 160, 1 62 -3, 164, 166 Cretaceous - Tertiary, 199, 203 - 4 Miocene, 86 end-Ordovician, 183, 1 83 end-Perrnian, 1 90, 191 , 192, 193 Pleistocene, 208 - 9 end-Triassic, 197 Vendian, 1 80 Lagerstatten, 291 molecular evidence, 220, 221 palaeopathology, 383 plant indicators, 354, 401 -3, 401 , 402 clines, reproductive isolation, 1 0 1 clinoid sponges, durability, 224, 225 clonal organisms, 43, 47, 331 clonopary, colonies, 330, 331, 331, 333 clonoteny, colonies, 330, 331, 333 Cloudina, 22, 24, 33, 34, 443 clubmosses, size, 1 50, 151 clypeasteroid echinoids, heterochrony, 114 cnidarians biomineralization, 27, 28, 29 colonies, 330, 331 , 333, 334 extinction, 1 89, 1 94 Lagerstatten, 271 , 2 72, 277, 279, 281, 282, 286, 287, 288 marine habitat, 64 Precambrian - Cambrian, 18, 2 1 , 22, 30, 32, 33, 44, 50, 51 , 180 see also coelenterates; corals coevolution, 1 3 6 - 8, 351, 368, 372, 373, 393, 494, 554 'co-opta tion', 1 45 Co-ordination, Principle of, 41 7 - 1 8

Index coal balls, Carboniferous, 264, 265, 352 coal beds, Permian, 1 92 coccoliths algae, 3 1 6, 3 1 6 diagenesis, 247 electron rnicroscopy, 509, 5 1 1 environmental indicator, 412 evolution, 1 2 1 , 1 2 3 extinction, 201 extraction techniques, 502 Lagerstatten, 283, 286, 288 Red Queen Hypothesis, 1 36 coefficient of drag, 324 coelacanths, 1 5 7 biogeography, 449 feeding, 366 Lagerstatten, 284 coelenterates colonies, 333 encrusters, 346 island faunas, 192 Lagerstatten, 279, 282, 286, 287, 288 Precambrian, 1 8 - 2 1 , 1 9, 20, 22, 23 size constraints, 1 49 see also cnidarians; corals coelobionts, encrusters, 349 coelobites, reefs, 342 Coelodiscus, 284 coelomate radiation, 50 Coe/ophysis, 363 coeloscleritophorans, Cambrian, 25, 34 exoskeleton, 26 coelurosaurs, feeding, 363, 374, 375 Colchester Coal Member, Illinois, 279, 280 Coleia, 284 Coleochaete, 63 coleoids, Lagerstatten, 284 coleoloids, problematic taxa, 443 coleopterans Baltic amber, 297, 297 coevolution, 138 predators, 373 collagen skeletons, 27, 98, 3 1 7 'collapse calderas', flattening, 287 collection management, museums, 5 1 7 - 9 coloniality, 2 1 , 330 - 5, 331, 332 encrusters, 346 - 7, 347, 349, 350 heterochrony, 1 1 7 colour, thermal maturity, 5 1 1 , 512, 513, 5 1 3 , 513, 514, 514 Colour Alteration Index, 275 Columbia River basalts, 178 combined gas chromatograph mass spectrometers (C-GC-MS), 96 comets, extinction process, 1 64, 1 65, 1 70, 1 77, 1 78 Comley, U . K . , Lower Cambrian, 277 commensalism, 138, 376, 380 Commission on Stratigraphy, International Union of Geological Sciences, 462, 465, 468 -9, 471, 476, 478 - 80, 482 communities, 551, 553 biofacies, 396 biostratigraphy, 485 evolution of, 391 - 4, 392, 393, 394 nomenclature, 426 succession, 392 compaction diagenesis, 248 Lagerstatten, 278, 283, 287 plants, 353

see also flattening competition adaption, 139 benthic habitat, 43 encrusters, 348, 439 - 50, 351 evolution, 1 19, 1 22, 124 extinction, effect on, 1 60 heterochrony, 1 15 predator diversity, 376 completeness of fossil record, 298 - 303, 298, 300, 301 , 302 compressions, plants, 245, 263, 264 Compsognatizus, 287, 363, 381 computer applications, 246, 3 1 2 - 3 , 326, 493 - 9 , 494, 496 documentation systems, collections, 5 18 - 1 9 concentrations, o f fossils, 235 - 7, 236 see also Lagerstatten concentration Lagerstatten, 267 - 8 , 269 concentration techniques, sample preparation, 504 Conception Group, southeastern Newfoundland, 1 7 conchiolin, bivalves, 223 concretions, diagenesis, 244, 245, 255, 284 concurrent range biozone, stratigraphy, 461 , 467, 467 condensation deposits, 269 condylarthrans, record, 86 - 7, 87, 137, 204, 204, 205 cone-in-cone pyrite, 255 confrontational strategy, encrusters, 347 congruent communities, 397 conifers evolution, 83, 1 9 1 , 197 hydrodynamics, 232 preservation, 264, 352 Conodont Alteration Index (CAI), 5 1 3 - 4 conodonts biomineralization, 25, 27 biostratigraphy, 461 , 467, 468, 479, 480, 484 extinction, 182, 1 83, 187, 194, 195 Lagerstatten, 274 - 5, 276 maturity, 5 1 1 nomenclature, 4 1 7, 420 - 1 , 420, 421 Ordovician, 479, 480 parasites of, 379 problematic taxa, 442 sample preparation, 502, 503, 504 thermal maturity, 513 - 4, 513, 51 4 Conomedusites, 18, 20 Conophyton, 1 79, 339 consecutive range biozone, stratigraphy, 461, 467, 467 consensus model, global diversity, 446, 447 conservation, stratigraphy, 474 conservation depOSits, 268 - 70, 269 conservation Lagerstatten, 277 consolidants, sample preparation, 501 -2, 501 constant generic associations (CGAs), 485 constructional morphology, 1 42, 310, 3 1 1 , 318 continental drift, 547 continental shelf, species diverSity, 133 continental uplift, extinction, 1 60, 1 64 conularids biomineralization, 25, 27 extinction, 189, 1 94 Lagerstatten, 279

Index Conulata, Precambrian, 18, 2 1 , 44 convergence, evolution, 1 42, 1 43, 435, 551 convex up-and-down orientations of shells, 226, 227- 8, 229, 258, 259, 260, 262, 281 Cooksonia, 62 'copal', amber, 294 Cope, E . D . , 543, 545 Cope's Rule, 1 15, 1 18, 1 50 copepods, parasites, 378 coprolites accumulations, 2 1 7, 257, 259, 267, 268, 292 dietary evidence, 362, 364, 365 - 7, 366, 372, 389 nomenclature, 424 parasitism evidence, 380 copulatory organs, terrestrialization, 68 coquinas, 54, 267, 269 coracoids, flight, 77, 78 coralline sponges, problematical fossils, 443 corals banks, 341 biofacies, 398, 399, 400 biomineralization, 26 colonies, 330, 333, 334, 335 destruction of, 224 diagenesis, 247, 248 diversification, 39, 40, 45, 46, 48, 54, 55, 56 encrusters, 347, 348, 349, 350 environmental indicators, 403, 406, 412 extinction, 1 60, 182, 1 83 , 1 84 - 5, 187, 1 89, 192 heterochrony, 1 1 3 Precambrian, 3 2 , 33 parasites of, 380 problematic taxa, 443 reefs, 288, 341 , 342, 342 , 343, 343, 345 scleractinian, 26, 1 89, 347 skeletons, 3 1 6 - 1 7 symbiotic, 1 38 trace fossils, 360 see also rugose corals ; tabulate corals Corbula, 388 cordaites, extinction, 191 Cordillera, North America, biogeography, 458, 458 coriaceous leaves, 231 Coriolis forces, 220, 221 Corixa, 321 cormidia, colonies, 332, 333 cornulitids encrusters, 347 symbiotic, 138 corrasion, 225 correlation see biostratigraphy corrosion skeletons, 223, 225, 226 taphofacies, 258, 258, 262, 263 'cortical bandages', graptolites, 442 corystosperms, c1adistic analysis, 80, 81 cosmic radiation, extinction, 1 64, 191 cosmopolitan species biogeography, 448 extinction, 456 - 7, 459, 460, 466, 467 Precambrian, 18 CosmorhopiJe, 359 Cot/IOn ion, 26 Cotylosauria, paraphyletic group, 433 'coupled logistic', model, diversity, 496 Cow Head Group, Newfoundland, 486

crabs brachyuran, 370 predation, 368, 369 terrestrialization, 66, 67, 68 craniacean brachiopods, heterochrony, 1 1 4 cratering, extinction evidence, 1 69 - 70, 177 cratonization, and stromatolites, 339 Crawfordsville crinoid beds, Indiana, 239 crayfish Lagerstatten, 287 terrestrialization, 67, 68 Creodonta, predators, 375 Cretaceous adaption, 142 angiosperms, 79, 80 - 3, 80, 83 biogeography, 455, 456, 457, 457, 459 biomechanics, 319 coevolution, 1 37, l 38 completeness of fossil record, 299 diagenesis, 253, 257 dietary evidence, 362, 363, 364, 366 - 7 diversification, 40, 4 1 , 48, 1 33 encrusters, 349 environmental indicators, 401 , 403, 404, 404, 410, 412 extinction compared other events, 193, 194 earth-bound causes, 1 60, 1 6 1 , 163 extra-terrestrial causes, 1 64, 1 65, 1 66, 1 67, 1 68, 1 68, 1 69, 1 69, 1 70, 553 marine, l 33, 198 - 203, 200, 400 periodicity, 171 - 2, 1 73 , 1 74, 1 75, 1 75, 1 76, 1 77 terrestrial, 4 1 , l 32, 133, 203 - 5, 204, 205, 206, 207-8, 400 flight, 76, 78 heterochrony, 1 1 5 Lagerstatten, 297 macroevolution, 127 molecular palaeontology, 98, 99 parasites, 378, 379 plant communities, 354 preservation, 264, 265 predation, 370, 371, 372, 375 size, 1 50, 1 5 1 source rocks, 222 stratigraphy, 465, 488 trace fossils, 361 terrestrialization, 67 trophic structure, 386 crinoids biofacies, 398, 399, 400 camerate, 160, 189 commensalism, 380 destruction of, 223 diversification, 38, 40, 45, 46, 47, 48, 54, 55 encrusters, 346 extinction, 1 60, 187, 189, 193 flattening, 246 hydrodynamics, 227, 229 inadunate, 1 60, 189 Lagerstatten, 239, 240, 267, 268, 269, 284, 288 prey, 372 reefs, 343 crocodiles bones, 234 diversification, 194, 1 95, 205, 206 evolutionary faunas, 39, 41 feeding, 366 - 7, 370, 375 Lagerstatten, 284, 292

563 size, 148 taphofacies, 259 Crocodylus, 234 Crocuta crocutu, 233 crowding, effect on extinction, 1 60 crustaceans biomechanics, 320 feeding, 362 Lagerstatten, 279, 280, 284, 288, 289 modern, 40, 48 predators and prey, 368, 369, 370 Precambrian, 2 1 terrestrialization, 65, 6 6 , 6 7 , 68 Cruziana, 362, 424 ichnofacies, 356, 357 - 8 , 358, 359, 361, 412 cryptalgalaminites, stromatoJites, 336 cryptic habitats, reefs, 342 cryptospores, evolution, 60, 61 cryptostomate bryozoans diversity, 1 89 extinction, 160 ctenophore, Hunsriick Slate, 279 Ctenostreon, 267 cubichnia, trace fossils, 355 cubomedusoids, Vendian, 32 Cucculaea, 283 cued testing, exhibit strategies, 521 - 2, 52 1 currents destructive process, 223, 226 Lagerstatten, 283 stromatolites, evidence from, 336 curvature, shells, 227 cuticle climatic indicators, 402 invertebrates, 27, 65, 318 plants, 60, 6 .1 , 62, 84, 231 , 241, 245, 351 cutins, diagenesis, 2 1 7 cuttlefish, hydrodynamics, 227 Cuvier, G . , ( 1 769 - 1832), 539 - 40, 540, 542, 543 cyanobacteria acritarchs, compared, 180 biomineralization, 24, 25, 26, 29 diversification, 49 - 50, 53, 54- 5, 56 Lagerstatten, 286, 287 nostocalean, 1 3 origin o f life, 7 Precambrian, 1 1 , 12, 13, 14, 15, 16, 30, 49, 51 reefs, 53 skeletons, 3 1 8 stromatolites, 336, 3 3 6 , 337, 338, 339, 340 terrestrialization, 57, 58, 59, 60, 63 cyanophytes, Vendian, 49, 50 Cyathocyatidae, completeness of record, 299 cycads climate indicator, 402 evolution, 81, 83 , 138, 191 Lagerstatten, 283 cyclocrinitids, problematic taxa, 443 cyclocystoid echinoderms completeness of record, 301 extinction, 1 8 1 Cyc/omedusa, 1 8 cyclostomes, encrusters, 347 Cyclozoa, Precambrian, 18, 1 9, 20, 21 Cymatiidae, predators, 390 Cymbosporites magll ificus Biozone, 466 cynoacryJate adhesives, specimen preparation, 501 , 502 Cynocephalus, 78

Index

564 cynodont therapsids predators, 373, 3 74 size, 151 Cyrtoceras Mudstones, 395 Cyrtograptus lundgreni Biozone, 463, 463 cystoid echinoderms completeness of record, 299, 300, 300, 301 extinction, 181, 1 83 obrution deposits, 239 Cystosporites, 422, 423 cytosol, Precambrian, 8, 15, 1 6

Dactyloteuthis, 284 Dakota Formation, Kansas, U . S . A . , 82 Dala peilertae, 276 Damaliscus, 234 Dapedium, 284 Dapedius, 364 Dart, R . , 545 Darwin, c . , (1809- 1882), 3, 9, 542, 543- 7,

552

'Darwinian fitness', 140 dasyclads, problematic taxa, 443 data handling, plant communities, 353-4 dating see geochronology Dawson, J.W., 545 Dawsonites, 6 1 , 63 de-watering, 251, 282 death assemblages, 237- 8, 238, 258 death marks, trace fossils, 355 debris flows, obrution deposits, 241 decay processes, 213- 16, 215, 2 1 6 Deccan Traps, India, 1 63, 1 78 DecheneIla rowi, 242 deciduous plants, climate indicators, 203 -4, 204, 402 Deep Sea Drilling Project (DSDP), 108,

404,

548, 549 deer, biomechanics, 320 'degenerate forms', heterochrony, 1 1 1 dehydration preservation, 270 terrestrialization, 69 Deinonychus, 375 Deinotherium, 543 Deltoideum delta, 5 1 0 'deme', microevolution, 125, 126, 126,

98- 9 detritus feeders evidence of, 362 Precambrian, 18, 22 trophic structure, 385, 386, 386, 386, 387 developmental processes, morphology, 309 Devonian biofacies, 396, 397, 400 coevolution, 137 completeness of fossil record, 299 diagenesis, 252, 255 diversification, 47, 45, 46, 47, 1 32 environmental indicators, 402, 405, 405,

41 1 evolutionary fauna, 40 extinction, 1 60, 1 67, 194 parasites, 378 - 9 plant communities, 352 preservation, 265 size, 151 predation, 370, 371, 3 71 , 372, 373 problematic fossils, 444 reefs, 55, 56, 345 stratigraphy, 466, 468, 475, 480- 2, 481 stromatolites, 340 taphofacies, 259, 260 terrestrialization, 58, 59, 60, 6 1 , 62, 63,

64, 65, 67, 68- 71 , 72, 75

see also HunsrUck Slate diacladogenesis, 394 diagenesis carbonate nodules and plattenkalks, 250- 3, 251 , 252 coprolites, 366 flattening, 244, 245 fossil concentrations, 236, 236, 240, 267,

268, 270, 283 Burgess Shale, 273-4 HunsrUck Slate, 278 - 9 Mazon Creek, 281 - 2, 281 , 282 'Orsten' deposits, 275 - 6 Solnhofen Limestone, 287- 8 fossil record, effect on, 445 iridium enrichment, 168 organic matter, 96, 97-8, 1 00, 217,

128,

129, 327

demosponges biomineralization, 25, 28 modem fauna, 38, 48 trace fossils, 360 dendrogram, systematics, 435 density, hydrodynamics, 323 deposit feeders bivalves, 400 modern, 48 Palaeozoic, 47 Precambrian -Cambrian, 22,

38, 41, 42, 43, 44, 45, 180 trace fossils, 356, 358, 359, 360 trophic structure, 385 , 386, 386, 388, 388, 389, 390 depth, indicators, 41 1 - 12, 41 1 , 412 Dermoptera, 78 desiccation preservation, 268 stromatolites, 337 terrestrialization, 60, 65 destructive processes, taphonomy, 224, 225, 226, 233, 237

determinants, immunological techniques,

223- 6,

219-20 phosphate, 256 - 7, 256 plants, 351 , 352 pyrite, 253- 5, 254 reefs, 343, 344 skeletal carbonates, 247- 50, 248, 249 trace fossils, 356, 357

diapsids, evolutionary faunas, 39, 41 diastrophism, extinction process, 1 60 diatoms electron microscope, 5 1 1 environmental indicators, 412 evolution, 121 stromatolites, 336 DiceIlograptus anceps, 478, 479 Diceras, 1 45 Dichoporita, extinction, 181 Dickinsonia, 2 0 , 21, 33 Dickinsoniidae, 21 dicotyledonous plants, 82, 85 Dicroidium flora, 197 Dictyonema, 3 79 Dictyonina, 2 73 dicynodonts predators, 373 size, 151

diet evidence of, 293, 362- 7, 363, 365, 366 see also coprolites digits, horses, 86 differentiative heterochrony 1 1 1 , 1 1 7 see also coprolites Dilleniidae, 81 Dimetrodon, 373 dinocephalians, size, 151 dinoflagellates Cretaceous, 201 thermal maturity, 513, 514 Dinosaur Provincial Park, Alberta, 204, 205 dinosaurs angiosperms, effect of, 81, 83 biomechanics, 320 evolutionary faunas, 39, 41 extinction, 194, 1 95, 202, 203, 204- 5, 205,

206, 207-8 feeding, 268, 363-4, 366, 367, 370, 373, 374 - 5 , 374 flying vertebrates compared, 76, 78 gastroliths, 363, 364 heterochrony, 1 14 palaeopathology, 381 , 382 radiation, 194, 195, 1 95 saurischian, 374- 5 size, 147, 148, 1 50, 1 50, 1 5 1 skeletons, 234, 382 theropod, 1 14, 374 see also archosaurs; ceratopsian dinosaurs; ichthyosaurs diphyletic, tetrapods, 69 Dipleurozoa, Precambrian, 21 Diplocraterion, 359, 360 Diplodocus, 148, 1 50 diploporitids diversification, 46, 47 extinction, 181 Diploria, 343 dipnoans feeding, 366 terrestrialization, 69 Diprotodontidae, extinction, 208 dipterans Baltic amber, 296, 296, 297 coevolution, 1 38 disarticulation, Lagerstatten, 283 'disaster forms', Tertiary, 201 disease, study of, 381 - 4, 382, 383, 384 dispersal ability, evolutionary rate, 157 biogeography, 448, 455-6, 455 colonies, 331 plants, 60, 64, 82, 83 dissolution, skeletons, 223, 225, 258 distance communication, exhibit strategies, 519-22, 521 divergent upward, stratophenetics, 440 diversification angiosperms, 79 Cambrian, 34 data, and nomenclature, 426 patterns, 1 30-5, 1 3 1 , 1 32, 1 34 adaption, due to, 141 - 2 Precambrian, 1 7, 1 8 , 22 see also evolutionary faunas diversity analysis of, 445- 8, 446 biofacies, 398, 399 brackish water, 407 colonies, 334, 339 community groups, 393, 394, 394

Index computer analysis, 495, 496, 497 encrusters, 350 predation, 376 trace fossils, 357, 360, 361 'diversity-pump hypothesis', 457 DNA fragment preservation, 99 genetic analysis, 327, 328, 329 heterochrony, 1 18 molecular palaeontology, 95, 1 53, 154 Dob's Linn, Scotland, 182, 479 - 80, 479 documentation systems, museum collections, 5 1 7 - 9 dogs, predators, 375 dolomite, stratigraphy, 476 dolomitization, 249 - 50 domical stromatolites, 336, 337, 337, 338, 338, 339, 340

domichnia, trace fossils, 356 Dominican Republic, amber deposits, 297, 297

Dorygnathus campylognathoides,

284

Doushantuo Fonnation, Yangtze Gorges, China, 3 1 Downton Castle Sandstone, Shropshire, 480, 481

drag, hydrodynamics, 323, 324, 324 drilling, predation, 369 - 70, 371 - 2

Drosophila,

1 0 1 , 1 02, 1 03, 104

drought avoidance, land plants, 60 DSDP (Deep Sea Drilling Project) cores, 108, 404, 546, 548

Dubois, E . , 544 Duck Creek Dolomite, Western Australia, 13

Dunham, Sir Kingsley, 469 durability, skeletons, 223

Durania,

1 45

durophagous predation, 38, 42, 47, 368, 370, 371 , 372

dust proofing, specimen storage, 5 1 6 dwelling structures, trace fossils, 355 - 6 dyads, terrestrialization, 60 - 2 , 6 1 dynamiC viscosity, hydrodynamics, 323 'dynasties', compared evolutionary faunas, 37 see also megadynasties dysaerobic environment biofacies, 397 environmental indicators, 409, 410, 4 1 0 extinction, 1 8 2 LagersUitten, 270 taphofacies, 259, 259, 260, 2 6 1 ear, vertebrates, 70 earthbound extinction processes, 1 60 - 4, 161

earthworms, terrestrialization, 65, 6 7 eburnation, bones, 382

Eccentrotheca,

27

ecdysis biomineralization, 26 terrestrialization, 68 echinodenns biomineralization, 25, 26 completeness of record, 299, 300, 300, 301 , 301

cyclocystoid, 181, 301 destruction of, 223, 224, 225 diagenesis, 247, 248, 250 diversification, 46, 47, 46, 89 environmental indicators, 406

eocrinoid, 38, 39, 45, 46 Euechinoidea, 433 extinction, 1 75, 1 8 1 , 1 8 3 , 187, 187, 1 89, 192

feeding, 389 LagersUitten, 239, 240, 242, 243, 281, 282, 283

Burgess Shale, 271, 272 HunsrUck Slate, 277, 278, 2 78, 279 Solnhofen Limestone, 286, 288 marine habitat, 64 parasites of, 378, 3 79 pelmatazoan, 54, 1 87, 1 89, 233 Precambrian-Cambrian, 22, 33, 34, 45 preservation, 268 - 9 size constraints, 1 49, 150 skeleton, 3 1 5 - 16, 318 stelleroids, 38, 46 stereom, 26, 62, 3 1 5 - 6, 3 1 8 trace fossils, 360 see also asteroids; crinoids; cystOid echinodenns; echinoids; edrioasteroid echinodenns; holothurians echinoids biofacies, 397, 400 clypeasteroid, 1 1 4 feeding, 389 heterochrony, 1 13, 1 14, 1 15, 1 1 6, 1 1 7, 1 1 7 Lagerstatten, 268, 270, 283 modern fauna, 38, 40, 46, 48 neolampadoid, 1 1 4 oxygen isotope ratios, 403 paraphyletic groups, 443 saleniid, 1 1 4 skeleton, 314 spatangoid, 115 tiarechinid, 1 14

Echinus,

300

echiurans, trace fossils, 360 echiuroids marine habitat, 64 Precambrian, 18 ecology, 548 biofacies, 396 - 7, 396, 397 evolutionary units, 393, 393 infonnation, fossil concentrations, 235,

macroevolution, 1 25, 126 microevolution, 1 0 1 , 1 05 reef, 341 , 342 economic success, selection, 126, 1 27, 128, 236, 236

129

ecophenotypy, computer analysis, 498 ecostratigraphy, 472 ectocochleates, biomechanics, 320, 321 ectomycorrhizae, terrestrialization, 59 ectothennic predators, 374, 3 74 Edentata, extinction, 208 Ediacara Hills, South Australia, 44, 548 Ediacaran see Vendian

Ediacaria, 18, 1 9 Edmondia, 281 Edmontosaurus, 205,

207

edrioasteroid echinodenns completeness of record, 299 encrusters, 347 extinction, 1 8 1 heterochrony, 1 14, 1 1 5 obrution deposits, 239, 240 Palaeozoic, 46 'effect hypothesis', selection, 127, 152 eggs

565 composition, 314, 3 1 8 terrestrialization, 7 0 El Kef, Tunisia, standard boundary sequence, 199, 2 00

Elasenia,

18

elasmobranchs, extinction, 1 89 Elbobreen Fonnation, Spitsbergen (Svalbard), 1 1 Elburz mountains, Iran, 476, 477

Eldonia,

2 73

electrical discharge, origin of life, 5 electromagnetic separation, sample preparation, 504 electron donors, decay processes, 2 1 3 electron microscopy, 508 - 1 1 , 5 1 0 electrophoretic techniques, 9 6 , 1 0 1 Eleonore Bay Group, East Greenland, 1 5 elephants palaeopathology, 383, 383, 384 size, 1 47, 1 50, 1 5 1

Elephas, 148,

150

Ellis Bay Formation, Anticosti Island, Canada, 479 elongation, shells, 227

Elonichthys peltigerus,

281

embryology, evolutionary systematics, 435 emigration, speciation, 108 empirical model, global diversity, 446 - 7, 446

encrusters, 237, 341 -2, 346 - 5 1 , 347, 348 endemic species biostratigraphy, 484 extinction, 456, 459, 460 endobionts, encrusters, 346 endocochleates, biomechanics, 320, 321 endolithic algae, effect on shells, 224, 248 endomycorrhizae, terrestrialization, 59 endoskeletons, Cambrian, 24, 26 endosymbionts, Precambrian, 16, 22, 23 endotherrnic predators, 373, 374, 374 energy Lagerstatten, 241, 290 origin of life, 5, 6 Red Queen Hypothesis, 120 taphofacies, 258, 258, 259, 260, 261 , 262, 263

trophic structure, 385, 389 enteropneusts, trace fossils of, 360 enterospirae, 366, 366

Entobia,

360

environment conditions animal size, 1 5 1 evolution rate, 1 5 6 heterochrony, 1 16 molecular fossil evidence, 96, 100 indicators climate from plants, 401 - 3, 401 , 402 depth from trace and body fossils, 4 1 1 - 2 , 41 1 , 412

oxygen levels from biofacies and trace fossils, 408 - 10, 4 1 0 salinity from faunal analysis and geochemistry, 406 - 8, 40 7 temperature from oxygen isotope ratios, 403 - 5, 404, 405 enzymes, genetic analysis, 327

Eoanthropus,

544

Eocene biofacies, 400 biogeography, 450, 451 decay processes, 2 1 4 diagenesis, 253, 254, 254, 255

566

Index

dietary evidence, 364, 367 environmental indicators, 404, 404, 405, 41 1

extinction, 161, 167, 169, 1 70, 1 73 , 1 74, 1 75, 1 76, 177 flight, 78 grasslands, 84, 85, 86 obrution deposits, 241 parasites, 377 predation, 370, 375 Red Queen Hypothesis, 121 size, 150, 151, 1 51 stratophenetics, 441 terrestrialization, 67 trophic structure, 389, 389 Eocoelia, 392 eocrinoid echinoderms, Palaeozoic, 38, 39, 45, 46 Eohippus, 544 Eohostinella, 62 Eoporpita, 18, 1 9 Eosphaera, SO, 5 1

eosuchians, range, 205, 206 Eosynechnococcus moorei, 57 epeirogenic changes, extinction, 163 Ephemeroptera, flight, 72, 73 -4, 73 epibionts, 239, 346 epifauna, 41, 42, 43 extinction, 185 modern, 48 Palaeozoic, 38, 45, 46, 47 Precambrian, 22, 33, 45 trophic structure, 385, 386, 387 epiphytes encrusters, 349 terrestrialization, 63 Epiphyton, 54

epizoans encrusters, 349, 350 parasitic, 380 epoxy resin, SEM, 509, 510 Equidae, 86- 7, 87 equilibrium experimental morphology, 308, 309 model, global diversity, 446, 446, 447 Equisetites, 283 Equus, 86, 208 Eremotherium, 207 ernietiids, Vendian, 21, 33 Ernietta plateauensis, 21 Eryon, 286, 366 erythrosuchids, predators, 373, 3 74 escalation, predation, 368 escape traces, trace fossils, 356 Esocidae, biogeography, 449 Essex fauna, 279, 281 , 282 Essexella asherae, 281

ethylene diaminetetracetic acid, specimen preparation, 501 eubacteria origin of life, 7 Precambrian, 12, 53 terrestrialization, effect on, 63 Eucalyptocrinites caelatus, 379 Euechinoidea, 433 eukaryotes extinction, 1 79 origins of, 7, 13, 1 5 - 1 6, 30, SO, 5 1 , 53 stromatolites, influence on, 337, 340 Euplococephalus, 205, 207 Euramerican plate, 71 Eurhinosaurus, 284

Europolemur koenigswaldi, 292

euryhaline environment environmental indicators, 406, 407 fish, extinction, 189 eurypterids biomechanics, 320, 320, 321, 322 extinction, 189 feeding, 370 Lagerstatten, 279 terrestrialization, 65, 66, 67 eurytopic taxa, 128, 158 - 9, 160, 258 Eusmilus, 381 eutherian mammals, predators, 375 Euthynotus, 284 euxinic condition decay processes, 213, 214 Lagerstatten, 283 evaporite deposits Cambrian, 35 Permian, 188, 192 event stratigraphy, 472, 474, 478 Everglades (National Park), Florida, 408 evergreens climate indicators, 401 , 402 forests, decline, 204 leaves, hydrodynamics, 230 Evmiaksia, 18 evolution adaption, 139 cladists, 429 classification, 422, 425 - 6, 432, 435 floras, 39, 40, 41 novelty, 435 rates, and biogeography, 456 'synthesis', 124 systematics, 434 - 7, 436 theory of, 3 evolutionary faunas marine, 37-40, 38, 39 terrestrial, 39, 40- 1 exaerobic facies, 409, 4 1 0 'exaptation', adaption, 145, 146 excretion, terrestrialization, 65, 69 exhibit strategies, 519-22, 521 Exogyra, 283 experimental approaches, morphology, 307 - 9, 308 extinction adaptive gaps, 137 angiosperms, 82 benthic species, 1 1 0 biogeography, 459, 460 community groups, 393 computer analysis, 495, 497 data, and nomenclature, 426 diversification, effect on, 37, 39, 40, 42, 47-8, 133, 134 diversity analysis, 447- 8 earth-bound causes, 160- 4, 1 6 1 events, effect o n reefs, 52- 3 parasitic hosts, 380 periodicity, 1 71 -8, 1 72, 1 73, 1 74, 1 75 physical environment, 1 19, 167-70, 1 68, 1 70

rate, 136, 185, 186, 186, 553 size, effect of, 151, 152 speciation, 128 Vendian, 1 7, 22-3, 33, 44, 1 79 -80, 1 80 see also extra-terrestrial cause; Red Queen Hypothesis extra-terrestrial cause, extinction, 1 19, 164- 70, 1 68, 1 69, 171 - 2, 1 77, 182,

191, 198, 553 extraction techniques, microfossils, 502- 4, 503

Extraordinarius Band, Dob's Linn, Scotland, 479, 480 Exxon sea-level changes, 161 eyes, experimental morphology, 308 F1 hybrid individuals, 101, 102, 103 fabricational element, morphology, 311 facies studies plants, 353 trace fossils, 362 faecal pellets see coprolites Fagus, 265, 231 , 232 Fahrenholz's Rule, 138 Falites, 2 75

false rings, trees, climate indicator, 402 Famennian extinction, 184 - 6, 186 red beds, East Greenland, 68 family level diversity, 1 34 immunological techniques, 99 farming systems, trace fossils, 356 faros, Silurian-Devonian, 56 n-fatty acids, organic components, 219 'Faulen', Solnhofen Limestone, 286 faunal association, 396 favositids, reefs, 55 Favreina, coprolites, 366 feathers, classification, 436 fecundity, colonies, 332 - 3 feeding adaption, 143 burrows, trace fossils, 356 Cambrian, 23 evidence of diet, 362- 7, 363, 364, 365 Precambrian, 22, 23 trophic structures, 385- 90, 385, 386, 386, 387, 388, 389, 390

felids, extinction, 208 fenestra ovalis, terrestrialization, 70 ferns extinction, 203 hydrodynamics, 232 terrestrialization, 40, 63 fertilization angiosperms, 82 terrestrialization, 65 fibrous habit, aragonite, 315, 3 1 5, 317 field emission, SEM, 511 Fig Tree Group, South Africa, 10, 51 , 53 filamentous fossils, Precambrian, 10, 12, 53 filter feeders extinction, 184, 193 Lagerstatten, 276 Precambrian, 18 size constraints, 149 trophic structure, 386 fire extinction, 203 - 4 hominid, 88, 89, 90 First Appearance Datum (FAD), 478 First Reviser, Principle of, 417 fish acanthodian, 185 biogeography, 449, 450, 450, 451 biomechanics, 320, 321 cichlid, 308 chondrichthyan, 38, 40, 148, 366

567

Index diversification, 38, 40 environmental indicators, 406 extinction, 185, 189, 1 94 feeding, 364, 366, 369, 370, 371 heterochrony, 1 18 Lagerstatten, 270, 279, 280, 284, 287, 288, 292 osteichthyan, 38, 40, 69 placoderm, 148, 185, 194, 279, 370 sample preparation, 502 size, 148 taphofacies, 259 tetrapod relationship, 69 see also teleostean fishes 'fitness', adaptation, 140 flattening, fossils, 244 - 6, 244, 246, 253, 279, 287 flatworms, terrestrialization, 65 'fliesen', resin, 296 flight aerodynamics, 325 arthropods, 72- 5, 73 biomechanics, 319, 320 experimental morphology, 307 vertebrates, 75- 8, 77 Flinders Ranges, South Australia, 31 -2, 33 'Flinze', Solnhofen Limestone, 286 floating theory, flight, 74, 75 'floats' , graptolites, 52 flood basalt, Cretaceous, 1 63 flora see plants Florida Bay, reefs, 343, 344 flowering plants see angiosperrns fluorapatite, diagenesis, 257 fluorescence, thermal maturity, 5 1 1 , 512- 13, 5 1 3 , 513 fluoridization, extraction techniques, 504 fluorine, diagenesis, 256, 257 fodinichnia, trace fossils, 356 folding, geochronology, 483 food supply benthic habitat, 42, 42, 43 hominids, 88, 90, 91 size advantage, 151 terrestrialization, 68 trace fossils, 356 trophic structures, 385, 386 Foraminifera biogeography, 457, 458, 458, 457, 487- 8 biomineralization, 2 5 biostratigraphy, 461, 462, 467 Cambrian, 52 diagenesis, 247, 248, 250, 256 electron microscopy, 509, 5 1 0 encrusters, 346, 3 4 7 , 348 environmental indicators, 403, 404, 404, 406, 407, 409, 41 1 , 412 evolution, 121, 1 2 3 extinction, 1 60, 1 84, 187, 189, 191, 198, 199, 200 fusulinid, 1 60, 189, 458, 458 Lagerstatten, 283, 288 parasitic, 380 phylogenies, 427 Red Queen Hypothesis, 1 36 reefs, 342, 342, 343 sample preparation, 504 speciation, 1 08 use of, 220 forelimbs, flight, 78 forests, fossil, 264, 266, 352 form genus, plant fossils, 422

formation, stratigraphy, 462 formative education, exhibit strategies, 521 - 2, 521 formic acid, sample preparation, 502, 503 fossil assemblage, 237, 238 see also obrution deposits fossil concentrations, 235 - 7, 236 see also Lagerstatten fossil forests, 264, 266, 352 fossil fuels, study of, 96, 100 fossil record, completeness of, 298- 303, 298, 300, 301 , 302, 388 Fossil-Lagerstatten, 235, 266 see also Lagerstatten

Fossundecima konecniorum,

280

founder effect, speciation, 103 Fourier analyses, extinction data, 1 72, 174 - 5 fractures, bone, 381 -2, 384 fragmentation destructive processes, 223 -4, 225, 226, 237 taphofacies, 258, 258, 259, 260 - 1 , 262, 263

framboids, diagenesis, 255, 266 Francis Creek Shale Member, Illinois, 279- 82, 280, 281 , 282 Frankfort Shale, New York, 240 Frasnian, extinction, 37, 40, 161, 184 - 6, 1 86, 400 freezing, preservation fossils, 268 frequency curves, fossil record, 301 -2, 302 freshwater diagenesis, evidence from, 252, 255 extinction, 185 taxa, 406, 407, 407, 408 trace fossils, 361 fringing reefs, 56 frogs, Lagerstatten, 292 frost rings, trees, climate indicator, 402 Froude number, 320, 321 fruits angiosperrns, 82, 83 hydrodynamics, 231 fugichnia, trace fossils, 356 fugitive strategy, encrusters, 347 fulvic acid, organic matter, 217 functional element, morphology, 76, 3 1 1 fungi basidiomycete, 59 oomycete, 63 preservation, 216 terrestrialization, 59, 61, 63 furcula, birds, 77, 78 fusain, plants, 263, 264, 264, 265 fusulinid foraminifera biogeography, 458, 458 extinction, 1 60, 189 Gaia, concept of, 136 Galapagos finches, speciation, 1 05 galls, trilobites, 379 - 80 gametogenesis, colonies, 335 gametophytes, preservation, 264 Ganntour Basin, Morocco, 256 ganoids, Lagerstatten, 284 gas production, 220 gas vacuoles, graptoloids, 52

Gastrochaenolites,

360

gastroliths, dinosaurs, 363, 364 gastropods

biofacies, 400 biogeography, 454, 455, 455, 456, 456, 459

Cambrian, 34 coevolution, 137 commensalism, 380 destruction of, 223, 224 environmental indicators, 406, 412 experimental morphology, 309 extinction, 1 67, 187, 189, 194 feeding, 362, 368, 369, 369, 370 hydrodynamics, 227, 228, 229 Lagerstatten, 267, 279, 292 modern, 38, 48 muricid, 370, 371 , 372 naticid, 122, 137, 370, 37l, 372 parasitic, 378 prey, 369, 371, 372 prosobranch, 65, 66, 67, 68 radula, 362 reefs, effect on, 54 survivorship curves, 122, 389, 389 terrestrialization, 65, 66, 67, 68 zygopleurid, 189 see also snails Gaudry, A . , 543 Geiseltalles brown coal, East Germany, 214 gel electrophoresis, 327, 327, 328, 329 Geminospora lemurata Biozone, 466 genealogical hierarchy, 125, 126 generation time, rates of evolution, 156 generative paradigms, morphology, 309 generic level, immunological techniques, 99 Genesee Formation, New York State, 255 genet, colonies, 331, 332, 333, 335 genetics analyses, population studies, 326 -9, 327, 328, 329, 329

classification, 236 - 7 evolution, 153, 154 genetic drift hypothesis, 95, 109 history of, 546 - 7, 548 origin of life, 3, 6 regulation, heterochrony, 1 1 8 reproductive isolation, 101 - 2, 1 14 genotype evolution rate, 1 53 natural selection, 140, 141 origin of life, 6 - 7 populations, 329 see also speciation geochemical evidence, 10, 216 extinction, 164, 167-9, 1 68, 1 70, 199 geochemistry decay processes, 213 taphofacies, 258, 259 geochronology, 469, 471 , 474, 483 -4 amino acid dating, 97, 9 8 , 99, 100 geochronometry, 464, 465 geographical distribution evolutionary systematics, 435 speciation, 101, 103, 104, 105, 108, 127 geography, development of, 547 geomagnetic field, extinction, 1 63 geometry, fossil concentration, 235, 236, 236

geopolymers, formation of, 217, 218 Georgina Basin, northern Australia, 57 geotherrnal H2S, 49, 50 Gervillia, 283 Gesner, c . , (1516- 1565), 537

568

Index

Gila monster, 205 Gilboa fauna, New York, 68 gills suspension feeding, 142, 1 42 terrestrialization, 67 Ginkgo, 283, 422 biloba, 232 ginkgoes, 191, 232 Girvanclla, 54 glaciation extinction, 162, 183, 1 83 , 208, 209 Permian, 187, 190, 191, 192 Precambrian, 1 7, 50 isotope ratios, 403-4 molecular evidence, 220 Ordovician, 478 palaeopathology, 383 reefs, effect on, 344 sea-level, effect on, 488 Glaessnerina, 44 glauconite, extinction evidence, 169 Gleedon Chronozone, Welsh borderland, 463, 463 glide reflection, bilateral animals, 21, 23 gliding, flight, 75, 78 global cooling, extinction, 191, 192 global diversity, 445- 7, 446 global standard stratigraphy, 462 -5, 463, 464, 468, 472-5, 476 global boundary stratotypes 471 - 5, 472 Ordovician- Silurian, 478 - 80, 479 Precambrian- Cambrian, 475 - 8, 477 Silurian -Devonian, 480 - 2, 481 Global Stratotype Section and Point, (GSSP), 462, 463, 465, 468, 472 - 5, 476

Globidens, 363 Globigerina eugubina, 1 99 globigerinid species, extinction, 1 72 globines, metazoans, 17 Glochiceras, 287 Gloeothece coerulea, 57 Glossifungites ichnofacies, 356, 358, 359, 360, 4 1 2

glossopterids, evolution, 80, 8 1 , 191 Glossopteris, 2 6 5 , 366 Glossotheriul11, 207, 208 glycine, 98 Glyphaea, 366 glyptodonts extinction, 208 size, 150 Glyptograptus persculptus, 181, 478, 479, 480 Glyptotheriul11 , 208 Gmund horizon, southern Germany, 239 Gnathicl111 u S, 351 gnathostomes, terrestrialization, 69 Gnetales, evolution, 80, 81 goethite, extinction evidence, 1 69 'golden spike', stratigraphy, 462, 463, 463, 464, 465, 468, 482 , Gondwanaland biogeography, use of, 458 biostratigraphy, 485, 487 diversification, 134 glaciation, extinction, 162, 183, 1 83 , 187 IGCP project, 470 goniatitic ammonites biostratigraphy, 484 extinction, 189 Goniol11ya, 283 gorizont, stratigraphy, 462

GotllOgraptus nassa, 463,

464

gradualism, speciation, 107, 108, 109, 1 10 gradualistically derived species, 427- 8 Gramineae, Miocene, 84 Graminophyllul11, 84 Grand Canyon Series, 30 Grandagnostus jalanensis, 302 graphical representation, computer analysis, 493, 495 graptolites biofacies, 485, 487 biostratigraphy, 461, 462, 463, 466, 467, 468 coloniality, 330, 332, 333, 334 destruction of, 224 diversification, 38, 45, 46, 47, 51 , 52 electron microscopy, 509 environmental indicators, 412 extinction, 181, 183, 1 83 flattening, 246 floats, 52 gas vacuoles, 52 heterochrony, 1 15, 1 1 7 global boundary stratotypes, 478, 479, 479, 480, 481, 482 lineages, 428 nemata, 52 parasites of, 380 problematic taxa, 442 rhabdosomal stabilizers, 52 size constraints, 149 thecal spinosity, 52 tubothecae, 380 vanes, 52 webs, 52 grasses, preservation, 352, 354 grasslands, 59, 83, 84- 7, 85, 87 grazing marine habitats, 38, 42 biomineralization, cause of, 29 encrusters, 350 reefs, effect on, 53, 54, 56 source rocks, 221 stromatolites, effect on, 31 trophiC structure, 385, 390 terrestrial habitats, 83, 85 - 7, 87, 180, 354 trace fossils, 356, 361 Great Barrier Reef, 52, 345 Great Plains, North America, 86, 87 green algae biomineralization, 25 environmental indicators, 4 1 1 stromatolites, 336, 340 terrestrialization, 51 , 63 green bacteria, Vendian, 49 Green River Formation, Wyoming, 253, 364, 370 greenhouse effect, extinction process, 1 64, 1 65, 166 greenstone belts, Archaean, 10 greigite, diagenesis, 253 grinding techniques, preparation, 499 - 500 'group selection', adaptation, 141 growth banding, diagenesis, 248, 249, 249 population studies, 326 Grube Messel, West Germany, 289 -93, 290, 291 , 292, 2 93 , 365 Gryphaea, 108 Guadalupian extinction, 1 74, 1 75 guerilla strategy colonies, 334

encrusters, 347 Gulf of Mexico coast, fauna, 41 1 , 412 Gunflint Iron Formation, Ontario, 1 1 , 13, 50, 53, 336, 339, 548 Gunflintia minuta, 1 1 , 13 gut contents, dietary evidence, 364 gymnolaemate bryozoans, modern fauna, 40, 48 gymnosperms evolution, 39, 40, 138 resin, 295 size, 147, 148, 151 Gyronites Zone, 1 88 habitat adaption to, 141 - 2 diversity, effect o n extinction, 160, 185, 193, 198 evolution rate, 157, 158 islands, 349 hadrosaur extinction, 205, 207 feeding, 364 Haeckel, E . , 545, 547 haematoma callus, palaeopathology, 381 - 2 haemoglobins, metazoans, 31 Haldane's rule, 1 02 Halkieria, 45 halkieriids, Cambrian, 34, 45 Hallidaya, 18 halysitids, Ordovician, 55 Hamamelidae, compared Albian forms, 81 Hamelin Pool, Shark Bay, Western Australia, 3 3 7 Hamilton Group, New York State, 259, 260 hand axes, hominids, 89 - 90 Haqel Limestone, Lebanon, 253 hard parts, flattening, 244 Harland, W . B . , 469 Harlaniella, 34, 180, 1 80 Hawaiian Islands, 192, 457 hearing, terrestrialization, 70 heat conservation, size advantage, 151 heat, effect on fossil molecules, 96 'heavy water', Cambrian, 35 hederellids, encrusters, 347 Hedinapis fauna, 398 heliolitids, Ordovician, 55, 182 Hell Creek Formation, Alberta, 204, 205 Helodermatidae, extinction, 205, 206 Helodus, 370 hematite, diagenesis, 259 Hemiaster, 1 1 5 hemichordates, marine habitat, 64, 2 72

Hemicystites parasiticus,

240

herbaceous plants, preservation, 352 herbivores, 373, 375 angiosperms, effect on, 83 evolution, 84, 85 - 7, 87, 137 herbs, habitats, 81 heredity, 'evolutionary synthesis', 124 Hesperornis, 78 Hesslandona unisulcata, 2 75, 276

Hesthesis immortua,

3 77

heterochrony, 1 1 1 - 1 18, 309, 498 heterocysts, Precambrian, 13 heterodont bivalves, 400 heterogametic sex, reproductive isolation, 102 heterogeneity, colonies, 335 heterotrophs evolution, 4, 5 - 6, 14, 16, 29

569

Index reefs, effect on, 53 heterozygosity individuals, 327, 327, 328, 328, 329 population, 328, 328, 329 reproductive isolation, 102 hexactinellid sponges, biomineralization, 25, 26, 27, 28 Heydenius an tiquus, 377 Heyden ius matutinus, 377 Hibbertopterus, 319 Hiemalora, 18, 20, 21

'Hierarchy theory', 125 - 9, 126 Highland Border Complex, Scotland, 484 Hildoceras, 283, 364 Hindeodella confluens, 421

hippo, teeth, 86 Hippurites, 145

Hirnantian fauna, 182, 183, 1 83, 478 see also Ordovician, extinction Historischer Aspekt, morphology, 311 history of palaeontology before Darwin, 537-42, 537, 538, 540, 541 , 542

Darwin to plate tectonics, 543 - 7, 544, 546

past decade and the future, 550 -5 plate tectonics to Paleobiology, 547 -50 Hjoula Limestone, Lebanon, 253 Holocene biofacies, 400 biogeography, 449, 451 coevolution, 137 grasslands, 86 nomenclature, 424, 426 - 7, 432, 433 parasites, 380 reefs, 344, 345 trophic structure, 390 holocephalians extinction, 189 Lagerstatten, 284 Holmesina, 208 holophyletic taxa, 39-40, 436 holosteans extinction, 189 Lagerstatten, 284 holostratigraphy, 469, 471 holothurians diversity, 46 Lagerstatten, 279, 281 , 282 trace fossils, 360 Holzmaden, West Germany, 270, 282 -4, 283, 284, 285

homeostasis, earth's surface, 136 hominids diet, 88, 89, 90, 91, 150, 208, 367 evolution, 88 -91, 89, 1 10, 144, 149, 428, 544 - 5, 544, 546, 547 jaws, 88, 90, 91 stratophenetics, 440, 441 Homo, 1 10, 1 49, 428 Homo Di/uvii Testis, Scheuchzer, J . , 539 Homo erectus, 88-90, 89 Homo habi/is, 88, 89 Homo sapiens, 89, 90 Homo sapiens neanderthalensis, 383 Homocrinus, 240

homoiohydry, terrestrialization, 60, 62, 64 Homonymy, Principle of, 417, 418, 424 homoplasy computer analysis, 497 evolution, 434, 435 Homotherium, 207, 208 Homotrema, 343

homozygous individuals, 327, 327 Hooke, R., (1635 - 1 703), 538, 539 hooved mammals, evolution, 86 - 7, 87 hopanoids, diagenesis, 218, 219 hormonal control, heterochrony, 118 'horotely', 153 horses evolution, 85, 86, 107, 1 18, 121, 138 extinction, 208, 208 feeding, 365 Lagerstatten, 292, 234 study of, 543 -4, 544, 545 Horseshoe Canyon Formation, Alberta, 204, 205 horseshoe crabs, living fossils, 157, 157 horsetails Lagerstatten, 283 size, 150, 151 Hostinella, 62 human evolution, see hominids humerus, flight, 76, 77 humic acid, diagenesis, 217 humidity, specimen storage, 515 - 6 Hungaia fauna, 398 Hunsriick Slate, 239, 245, 254, 269, 277- 9, 2 78

HunsrUckschiefer see Hunsriick Slate hunting, hominids, 88, 89, 90, 91, 208 see also feeding Huroniospora, 1 1 , 13, 50, 51 Huxley, T . H . , 543, 544, 544, 545 hyaenas, feeding, 367, 375 hyalosponges, extinction, 184, 185 Hyatt, A . , 545, 546 hybodonts, predation, 370 Hybodus, 284, 364, 3 65 hybrid zones, reproductive isolation, 101 Hydra, 333 hydrocarbons source rocks, 217-8, 220 - 1 , 221 thermal maturity, 512, 514 hydrochloric acid, sample preparation, 502, 504 hydroconozoans, biomineralization, 25, 26 hydrodynamics, 322 - 5, 324, 325 decay, 214-5, 2 1 6 information from concentrations, 236, 236, 237 obrution deposits, 241 reefs, 344 transport, 227-9, 228, 229 hydrofluoric acid, extraction techniques, 504 hydrogen peroxide, sample preparation, 500, 503 hydrogen sulphide diagenesis, 253, 254, 255 Lagerstatten, 271, 279, 292 origin of life, 12 Precambrian, 49, 50 hydrolyzation, organic debris, 95 hydrostatics, 322 skeletons, 67, 314, 320 hydrothermal metamorphism, Cambrian, 36 hydrothermal vents, origin of life, 8 hydroxy-fluorapatite, diagenesis, 256 hydroxyapatite, diagenesis, 256 hydrozoans coloniality, 330, 334 Lagerstatten, 279 Vendian, 44 Hylochoerus, 234

Hylonomus, 70, 71

hymenopterans Baltic amber, 296 - 7, 297 coevolution, 138 hyolithelminths biomineralization, 27 problematic taxa, 443 hyoliths Cambrian, 25, 25, 34, 38, 39, 45, 272, 273 problematic taxa, 442, 443 hypermorphosis, 1 1 1 , 1 12, 1 1 3 , 1 14, 1 1 7, 118 hypersaline taxa, 271, 407, 407 see also salinity hypocleidium, 78 Hypohippus, 86 hypsilophodonts, extinction, 205, 207 hypsodont teeth, grazers, 86, 87, 138 Hyracotherium, 86 Iapetus, biostratigraphy, 485, 486, 489 Icaronycteris, 78

ichnofacies, 356 - 60, 358, 359, 360 ichnofossils see trace fossils ichnological nomenclature, 423 - 5 Ichnusina, 1 8 lchthyornis, 78 ichthyosaurs classification, 435, 436 feeding, 363, 364-5, 370, 372 Lagerstatten, 284, 285 skeleton, 382 taphofacies, 259 Ichthyostega, 69, 69, 70 ichthyostegalians predators, 373 terrestrialization, 68 -9, 69, 70 Ichthyostegopsis, 68 -9 19uanidae, 205, 206 Iguanodon, 366, 543 iguanodonts, 543 feeding, 364, 366 Illinois, marine reef, 55 - 6 Ilyanassa obsoleta, 390 image analysis, 498 immunological techniques, molecular fossils, 98- 9 Imperato, F . , (1550 - 1625), 538 inadunate crinoids, extinction, 160, 189 inarticulate brachiopods taxonomy, 433 Triassic, 192 incertae sedis, nomenclature, 423 index fossils, 295, 461, 466 - 7, 466, 467 Indo-west Pacific region, species richness, 456, 457 lndricotherium, 149, 150 infauna, 41, 42, 42, 43 Cambrian, 38, 45 modern, 48 Palaeozoic, 47 Precambrian, 22, 33, 44 suspension feeding, trophic structure, 385, 386, 387 infections, skeleton, 382 -3 information, collections, 517- 18 inoceramid bivalves, extinction, 201 , 400 lnoceramus, 364 Inordozoa, Precambrian, 18, 21 insectivores, size, 150 insects adaption, 142

Index

570 apterygote, 65, 72, 73, 74, 297, 297 coevolution, 136, 137 - 8 flight, 72, 73, 74, 307 Lagerstatten, 268, 279, 288, 289, 297, 297 protopterygote, 72, 74 pterygote, 65, 321 speciation, 104 terrestrialization, 64, 65, 66, 67 intelligence, size advantage, 151 intensity of selection, 156 interactor, selection, 127 intercellular space, plants, 60 International Association for Plant Taxonomy (IAPT), 419 international bodies, 419, 470, 522

see also under individual names International Botanical Congress, 419 International Code of Botanical Nomenclature, 418, 422, 516 International Code of Zoological Nomenclature, 417, 418, 419, 420, 423, 516 International Commission on Stratigraphy (ICS), 468- 469 International Geological Congress, 476, 522 International Geological Correlation Programme (IGCP), 469 - 70 International Palaeontological Association (IPA), 470, 522 International Palaeontological Union (IPU), 522 International Union of Biological Sciences, 419 International Union of Geological Sciences (lUGS), 462, 465, 468 - 70, 471, 474, 476, 478 - 80, 482, 522 intransitive overgrowth, encrusters, 350 invertebrates coevolution, 137 diagenesis, 257 extinction, 200, 201 -2 genetic variability, 328, 328 size constraints, 149 - 50 terrestrialization, 64- 8, 66 ion balance regulation, terrestrialization, 65 iridium, extinction evidence, 1 63, 1 64, 165, 1 67, 1 68, 1 68, 169, 1 70 Cretaceous - Tertiary, 199, 203 Ordovician, 182 periodicity, 177 Permian, 191, 193 Triassic, 198 Irish Elk, biomechanics, 319-20, 3 1 9 iron decay process, 213, 216 diagenesis, 250, 251, 252, 2 5 2 , 253, 254, 255 Lagerstatten, 240, 273, 281, 282, 293 Precambrian, 12, 13 island faunas, 106, 193, 376, 457 isograptid biofacies, 485, 487 isomerization, organic compounds, 219 isometric growth, heterochrony, 1 1 1 isopods parasites, 378 terrestrialization, 66, 67, 68 isoprenoids, biomarker, 219 lsoptera, amber, 297 isotope data, 200, 201, 471 see also oxygen isotopes

Isua, southwest Greenland, Archaean, 12, 51

Kukalova americana, 73 Kullingia, 18

iteration, colonies, 330, 333, 334 Jaccard similarity coefficient, 453, 454, 454 Jameson, R . , ( 1774 - 1854 ) , 542 jaw articulation, classification, 436 jellyfish see Scyphozoa Joint Oceanographic Institutions for Deep Earth Sampling (JOIDES), 548 journals, 524- 9, 530 - 4 Juniata Formation, Pennsylvania, 58 Jurassic biofacies, 395, 400 biogeography, 458 coevolution, 137, 138 decay process, 214, 2 1 5 diagenesis 251, 251 , 252 dietary evidence, 362, 363, 364 -5, 366 diversification, 40, 41, 48, 133 flight, 78 Lagerstatten, 267, 268 microevolution, 108 molecular palaeontology, 98, 99 obrution deposits, 239 palaeopathology, 382 parasites, 378, 379 plant communities, 352 predation, 372, 3 74, 375 size, 150, 151 source rocks, 222 stratigraphy, 463, 465, 466, 488 taphofacies, 259 terrestrialization, 67 see also Holzmaden; Solnhofen Limestone K - T boundary event sequence, standard, 198 - 9 K-selection 1 15, 1 1 7 Kabwe, Zambia, 90 kangaroo, size, 150 kaolinite, Lagerstatten, 281 Karoo beds, South Africa, 373 karst surfaces, Ordovician, 182 karstic phenomena, reefs, 344, 344 Karweil type diagram, thermal maturity, 512, 5 1 2 , 5 1 3 Kazakhstan block, 187, 1 88

Kellibrooksia macrogaster,

280

kerogens Precambrian, 12, 13 source rock, 217, 218, 220 thermal maturity, 512, 514-5 Khorbusuonka Series, N orthern Yakutia, 17 Kilauea volcano, Hawaii, 167 Kildinella lop/lOstriata, 179 kinematic viscosity, hydrodynamics, 323 Klonk, Czechoslovakia, stratigraphy, 468, 481 , 482 Knightia, 364

Knightia eocaCll a , Knorria, 423

305

Konservat-Lagerstatten, 245 see also Lagerstatten Konstructionsmorphologie, 310, 3 1 1 Koobi Fora Formation, Lake Turkana, Kenya, 340 Korytnica Clays, Poland, 386, 388

labechiids, Femennian, 184 Labyrinthitos, 55 labyrinthodonts evolutionary faunas, 39, 41 extinction, 194 predators, 373 Labyrinthus, 26 Lagania cambria, 215 Lagerstatten, 34, 239, 240 - 1 , 243 266 - 70, 269, 380 effect on diversity, 445 and nomenclature, 426 see also Baltic amber; Burgess Shale; Grube Messel; Holzmaden; Hunsriick Slate; Mazon Greek; 'Orsten'; Solnhofen Limestone lagoonal conditions, 287, 345 Lake Tanganyika, 221 Lamarck, J . B . , ( 1744 - 1829 ) , and Lamarckism, 540, 544, 546 Lance Formation, Alberta, 204, 205 land bridges, theory of, 547, 549 land snails, speciation, 107 Laplandian glaciation, 17 Lapworthella, 44 laser disc technology, 497- 8 Last Appearance Datum (LAD), 478 lateral lobes, flight, 73 Latimeria, 157 Latirus moorei, 389, 389 latitudinal effect biogeography, 456 - 7, 457 extinction, 184 Laurasia, 134 Laurentia, 485, 487 Law of Constant Extinction, 1 19, 122, 136 Lazarus taxa, 1 66, 1 67, 189, 193, 299, 448 leaves angiosperms, 79, 80, 80, 81, 82, 83, 84, 85 climate indicators, 401 - 2, 402 hydrodynamic properties, 230 - 1 , 231 , 232 stomata, 60, 62, 231, 402 Lebensspuren, 356 lecithotrophic molluscs, biogeography, 455, 455, 456, 456 Leclercqia, 62 Lee Stocking Island, Bahamas, 337 leeches parasites, 378 terrestrialization, 65, 68 Leica 'R' system, photography, 507- 8 Leitz systems, photography, 505, 506 507-8, Lemuroidea, stratophenetics, 440, 441 leperditiid ostracods, extinction, 189

Lepidocarpon, 423 Lepidodendron, 151 Lepidophloios, 422, 423 Lepidophylloides, 423 Lepidoptera, amber, 297 lepidosaurs, Triassic, 194 Lepidostrobophyllum, 422, 423

Lepidostrobus, 423 Lepidotes, 284, 363 Lepisosteus, 157, 367 Leptoceratops, 205, 207 Leptoiepis, 284, 364

571

inaex Leptopterygius,

284 LevalIois technique, 90 level bottom communities, biofacies, 397- 8 Liaoning Peninsula, China, 339 lichens, analogues for bryophytes, 58 life assemblages, 237 -8, 238 life expectancy, hominids, 91 lift, hydrodynamics, 323, 324, 324 lignin decay, 214, 2 1 5, 217 diagenesis, 254 terrestrialization, 60, 63 limbs grazers, 86 hominids, 88 limestone Lagerstatten, 274, 275, 277 stratigraphy, 476 stromatolites, 336 see also Solnhofen Limestone Limestone-Dolomite 'Series', East Greenland, 1 1 limnic stagnation deposit, Lagerstatten 290 - 1 limonite coprolites, 366 permineralization, 266 Limulus, 157, 1 57, 319 lineages, 106, 127, 151, 1 54, 155, 427 -8, 473 linear form, encrusters, 347, 347, 350 Lingula, 98, 157, 302, 399, 4 1 1 Linnaean taxonomic classification, 108, 422, 426, 433, 539 Liopleurodon macromerus, 382 Liostrea, 283, 288 lipids diagenesis, 217-8, 2 1 8 origin o f life, 8 lissamphibians evolutionary faunas, 39, 41 predators, 376 Triassic, 194 Lister, M . , ( c . 1 638 - 1 712), 538 - 9 Iithistid sponges, Palaeozoic, 54 lithographic limestones, 252 - 3, 269 - 70 lithoherms, reefs, 341 , 342 - 3 Lithophaga, 343 lithostratigraphy, 462, 464, 471, 474 LitllOtiJamnion, 247 liverworts, terrestrialization, 60, 64 'living fossil', 1 52 - 3, 157-8, 1 58 lizards Cretaceous, 205 evolutionary faunas, 39, 41 Lagerstatten, 292 local range biozone, stratigraphy, 461, 467, 467 locomotion adaption, 143 biomechanics, 320 hydrodynamics, 325 mammals, 375 size, relationship to, 147 terrestrialization, 65, 70 trace fossils, 355, 356 Loliginites, 284 Loligosepia, 284 London Clay, Kent, 254, 254, 255 longevity biogeography, 459, 460 size advantage, 151

longitudinal diversity gradients, biogeography, 456, 457 Longport, New York, Lower Rochester Shale, 240 lophodonty, horses, 86 lophophorates, marine habitat, 64 Lorenzinia, 359 Lorenzinites, 18 Loripes, 388 Lorisoidea, 440, 441 Lovenia, 1 1 5 lucinid bivalves, trophic structure, 390 Ludlow Bone Bed, Shropshire, 480 - 1 , 481 Lumbricaria, 364 lungfish Lagerstatten, 279, 292 terrestrialization, 69, 70 lungs, terrestrialization, 67, 69 Iycopods, evolution, 40, 62 -3, 352, 354 Lycospora, 423 Lyell, c . , ( 1 797 - 1 875), 542 Iysigenic mode, resin production, 295

Maastrichtian extinction, see Cretaceous extinction Macm1Opsis, trace fossils, 358 Machairodontidae, predators, 151 mackinawite, diagenesis, 253 Macoma baltlzica, 229 macroevolution, 1 19, 124-9, 126, 550, 552, 553 macromolecular templating, origin of life, 4 macrophotography, 505, 507, 508 Macropodidae, extinction, 208 Macropoma man telli, 366 magnesium, diagenesis, 247, 248, 249 - 50, 257 magnesium : calcium ratio, sea water, Cambrian, 36 magnesium carbonate, biomineralization, 24, 26, 36, 264, 314, 315, 316 magnesium oxide, photography, 505 magnetite extinction evidence, 169, 1 70, 178 skeletons, 314 magnetostratigraphy, 461, 469, 471 , 472, 473, 474, 478 Magnoliales, flower, 82 malacostracans modern fauna, 38, 40, 48 terrestrialization, 66, 67 Mallophaga, coevolution, 138 mammals adaptive features, 145 classification, 436, 436 characteristics, 190 coevolution, 137 dentition, 363 eutherian, 375 evolution rates, 153 evolutionary faunas, 38, 39, 41 extinction, 204, 204, 207 - 9, 208 feeding, 365, 367, 375 heterochrony, 1 1 8 hooved, 86 - 7, 87 j aw, 320 Lagerstatten, 292 proteutherian, 204, 204 radiations, 106, 1 94 size constraints, 147, 148, 1 50, 151

speciation, 1 09 survivorship curves, 1 19, 120 terrestrialization, 68 mammoth extinction, 208, 208 feeding, 365 human int1uence on, 150 Lagerstatten, 268 Mammul, 208, 208

Mllnlmut/lllS jeffersoni, 208 primigenius, 208

manganese diagenesis, 251, 252, 252 oxidizing bacteria, 13 reduction, decay process, 214, 2 1 6 Manicougan crater, Canada, 198 manoxylic wood, climate indicator, 402 mantle plumes, extinction, 162, 163, 1 64, 167, 170, 1 78 marcasite, Lagerstatten, 291 Macoma, 389 marine environment, 4 1 - 8 benthic habitat, 42 -4, 42 , 4 3 , 44 coevolution, 137 diversity of species, 1 30, 131 - 2, 1 3 1 , 133, 134, 1 34, 135, 192 evolutionary faunas, 37 -40, 38, 39, 41 extinction, 189, 1 89, 1 90, 198 - 203, 200 faunal histories and ecological structure, 44 -8, 45, 46, 47 heterochrony, 1 1 5 Precambrian, 1 8 , 22 predation, 368 - 72, 369, 371 source rocks, 220 Marrellomorpha, Precambrian, 21 Marsh, O . c . , 543 -4, 544 marsupials extinction, 204, 204 predators, 376 Martil1ssol1ia e/ollgala, 2 75, 276 Marywadea, 21 mastodon, extinction, 208 mat building communities, 13, 1 5 mathematical modelling, 493 Matthew, W . D . , 546, 547 mating behaviour, reproductive isola tion, 101 martix algebra, use of, 246 matter -energy transfer, hierarchy theory, 126 maximal congruence, 434 mayflies, 72, 73, 73 -4 Mayr's allopatric speciation model, 107 Mazon Creek, Illinois, 72, 214, 2 1 5, 240, 279-82, 280, 281 , 282 Mecca Quarry Member, Illinois, 279 - 80 mechanical methods, preparation, 499 - 500, 500 mechanical strength, flattening, 244 Mecochirus, 288, 289 media communication, exhibit strategies, 520 - 1 developmental testing, exhibit strategies, 521 - 2, 52 1 Medicine Peak Quartzite, Wyoming, 30 'Mediterranean-like' basins, Cambrian, 35 medusae Lagerstatten, 279, 281 Precambrian, 18, 21, 30, 32 . 44, 50, 51 , 180

Index

572 Medusae Incertae Sedis, 424 Medusinites, 18 megadynasties, tetrapods, 373 - 6, 3 74 Megagrapton, 359 Megahippus, 86 Megalomoidea, 151

Megalonichidae, extinction, 208 Megalonyx, 207, 208 Megaptera, 321

megasporophyll, angiosperms, 80 Megatheriidae, extinction, 208 Meishucun, Yunnan Province, China, 476, 477 Melanorosaurus, 150 Meleagrine/la, 284 membranes, origin of, 8 Mendelian populations, 327, 546 'Mendelian revolution', 546 Mercati, M . , 538, 538 Merychippus, 86 Mesogastropoda, predators, 372 mesohaline taxa, 407, 407 Mesolimulus, 288 mesonychids, predators, 375 Mesozoic biofacies, 400 biogeography, 457 coevolution, 137 communities, 391 diagenesis, 250 dietary evidence, 363, 366 diversification, 40, 48, 132, 133, 1 34 encrusters, 347, 347 environmental indicators, 406, 408 molecular palaeontology, 97 parasites, 378 plant communities, 354 predation, 370, 372, 373 - 5, 3 74 size, 151 stratigraphy, 461 , 463, 467 terrestrialization, 67 Messel Lake, Germany, 241 messelite, Lagerstatten, 291 Messor barbarus, 233 metacarpus, flight, 76, 77 metacladogenesis, 394 metal tolerance, plants, reproductive isolation, 101 metamerism, Precambrian, 21, 23 metamorphism, effect on fossil record, 445 metaphytes Precambrian, 15, 16 problematic taxa, 443 metapopulation, colonies, 332 Metasequoia, 422 metazoans effect on stromatolites, 1 79, 339, 340 hard parts, origin of, 24 -9, 25, 28 Late Precambrian - Early Cambrian diversification, 30 -6, 32, 35, 44, 45, 180, 548, 549 parasites, 376 - 7 Precambrian, 1 5 , 1 6 , 17 - 23, 1 9, 2 0 meteoric environment, diagenesis, 248, 249

meteorites, extinction, 182, 198 methane decay product, 213, 214, 216 diagenesis, 251 , 252, 2 5 2 , 281 methanogens, biomarkers, 219 methylotrophy, Precambrian, 12- 13, 15 4-methylsteroids, biomarkers, 219 Metrarabdotos moniliferum, 5 1 0

Mialsemia, 20, 21 micritic deposits diagenesis, 248, 249 Lagerstatten, 285, 286 microarthropods, terrestrialization, 58, 59, 68 microbenthos, Precambrian, 13, 14 microbial decay, organic matter, 217 microbial mats decline of, 31 Metazoans, effect on, 1 79 stromatolites, 336, 339, 340 terrestrialization, 57, 58 microbial soils, terrestrialization, 57- 8, 58, 59 Microdictyon, 25, 27 microevolution, 106 - 1 10, 1 09, 1 19, 124 microfossils Archaean, 10- 12, 1 1 , 50 cyanophytes, 49, 50 extraction techniques, 502- 4, 503 evolution, 121, 1 23 grasslands, 84 lineages, 428 problematic taxa, 443 - 4 spheroids, 1 0 , 1 1 , 1 2 , 1 4 stromatolites, 338 study of, 461 , 549, 553 micropalaeontology see microfossils microplankton, 1 99, 200 microsporophyll, angiosperms, 80 Microsy o poidea, evolution, 440, 441 microtektite horizons, extinction evidence, 167, 169, 1 70, 1 77 migration, speciation, 108 millipedes Lagerstatten, 279 terrestrialization, 65 mineral surfaces, origin of life, 5, 8 mineralization decay process, 213, 214, 2 1 5, 216 diagenesis, 253-4 oxygen, effect on, 409 skeletons, 24, 97, 224, 317-8, 339- 40 mineralogical evidence, extinction, 169 Miocene angiosperms, 83 biofacies, 500 environmental indicators, 404, 404, 405, 409, 410, 4 1 1 extinction, 1 70, 1 73, 174, 1 74, 1 75, 1 76, 177 grasslands, 84, 85, 86 macroevolution, 128 microevolution, 109 molecular palaeontology, 98, 99 parasites, 378 predation, 370, 375 Red Queen Hypothesis, 121 size, 1 51 trophic structure, 386 - 7, 387 Miohippus, 86 Mioplusus, 364 labracoides, 305

Mistaken Point Formation, southeast Newfoundland, 31, 32 - 3, 32 mites, terrestrialization, 58, 59, 65 mitosis, heterogeny, 1 1 8 mitotic heterochrony, 1 1 1 , 1 13, 1 17, 1 1 8 Mivart, G . , 546 moa, size, 149, 150 Mobergella, 25, 27, 371 modules, colonies, 333

Moffat Shale Group, Dob's Linn, Scotland, 479- 80, 479 molars, hominids, 90 molecular clock hypothesis, 31, 95, 155 molecular palaeontology, 95- 100, 97, 98, 153 -4, 155, 548 metazoan evolution, 31 population studies, 326 Cambrian, 22, 25 terrestrialization, 64 molluscs biofacies, 398, 399 biogeography, 455, 455, 456, 456 biomineralization, 25 coevolution, 137 destruction of, 224, 225, 226 diagenesis, 255 expansion, 187, 189 extinction, 162, 187 environmental indicators, 408, 409, 4 1 1 , 412 feeding, 362, 368, 369, 371 heritability, 127 heterochrony, 113 hydrodynamics, 227, 228 - 9 Lagerstatten, 271, 272, 277, 279, 281 lecithotrophic, 455, 455, 456, 456 monoplacophoran, 38, 39, 45, 273 morphology, 3 1 1 periostracum, 25 planktotrophic, 455, 455, 456, 456 predators, 368, 369, 371 prey, 372 problematic taxa, 443 size constraints, 149 - 50, 151 skeletons, 317, 318 speciation, 108, 192 survivorship curves, 389, 389 taphofacies, 259 see also ammonites; amphipods; belemnites; bivalves; cephalopods; gastropods monads, terrestrialization, 60, 6 1 , 62 monocotyledons, Cretaceous, 81 Monocraterion, 359

monogeneans, parasites, 377 Monograptus ludensis, 463, 464 Biozone, 466 Monograptus transgrediens, 481 Monograptus ultimus, 481 Monograptus u niformis, 481 , 481 , 482

Biozone, 468 monophyletic groups cladistics, 43 1 , 432 computer analysis, 497 diversity analYSiS, 447, 448 problematic taxa, 443 taxonomy, 427, 428 tetrapods, terrestrialization, 69 monoplacophoran molluscs, Cambrian, 38, 39, 45, 273 Monopleura, 145 montane forests, fossil record, 83 Mon tastrea, 343

Monterey Formation, California, 409, 410 montgomeryite, Lagerstatten, 291 morphology, 307 - 13, 308, 3 1 0, 3 1 2 basis for nomenclature, 422 - 3 computer analysis, 497, 498 developments, 551 , 553 evolution, 153, 154, 155, 156, 156, 158, 550 flattening, 244

573

Index phylogenetic approaches 309 - 10, 3 1 0, 311, 312 similarity see stratophenetic classifica tion stratophenetics, 437, 438, 439, 439 mortality populations, 326 size advantage, 151 mosaic heterochrony, 1 1 7 mosasaurs extinction, 202 feeding, 363, 368, 369, 370 size, 148 motility, and biogeography, 455 moulting arthropods, 26, 68, 149, 317, 319 bradoriids, 27 mounting, palynological technique, 504 Mousterian, culture, 90 movement, vertebrate terrestrialization, 70 multielement, skeletal type, 225, 226 multituberculates, Tertiary, 204, 204

Murex ju/vescens,

369

muricid gastropods, predators, 370, 371, 372 muscles, relationship to size, 147 Musee National d'Histoire Naturelle, Paris, 549 museology, 515-22, 52 1 Museum Data Standard of the Museum Documentation Association (MDA), 519 museums, 529 - 30, 535 - 6 mussels, concentrations, 236 mutations, 100, 1 56 myacids, predators, 375 Myalina, 364 mycophagous feeders, terrestrialization, 58, 59 mycorrhizal association, terrestrialization, 59 Mylodontidae, extinction, 208 My/ohyus, 208, 208 myriapods predators, 373 terrestrialization, 65, 66, 67, 68 Myti/us, hydrodynamics, 228 Mytilus edulis, 229 myzostomids, parasitic, 378 nacre, skeletons, 25, 224, 225, 317, 318 Nama Group, Namibia, 17 Name-bearing Types, Principle of, 417, 418 Namibia, Vendian metazoans, 31, 33 Nannippus, 86 nannoplankton, 198, 199, 201 , 443, 549 nappes, biostratigraphy, 484 Nassariidae, predators, 390 Nassella, 84

Natica severn,

369

naticid gastropods coevolution, 137 predators, 370, 371 , 372 survivorship curves, 122 nautiloids amino acid profiles, 97 biomechanics, 320 Nau ti/us, 143, 157, 314, 316, 3 1 6 , 317, 321 Neanderthal man, 89, 90, 91, 381, 383, 544, 544

Nearest Living Relative (NLR), plants, 401 , 403

440, 441 necrolysis, LagersUitten, 268 necrosaurs, extinction, 205, 206 Nemagraptus gracilis, 479, Nemakit-Daldyn assemblage, Siberian Platform, 24, 25, 26- 7 nematodes habitat, 65 parasites, 377, 3 77 Precambrian, 31 size constraints, 149 trace fossils, 360 nematomorphs parasites, 377 trace fossils, 360 Nematophytales, terrestrialization, 6 1 , 62, 63 Nematoplexus, 63 Nematothallus, 6 1 , 62, 63 nemerteans habitat, 65 trace fossils, 360 'Nemesis', extinction cause, 177-8 Nemiana, 18, 1 9 neogastropods biofacies, 400 palaeobiogeography, 456 Neogene diversification, 48 grasslands, 85 microevolution, 108 taphofacies, 259 - 60 terrestrialization, 67 see also Miocene; Pliocene Neohipparion, 86 neolampadoid echinoids, heterochrony, 1 14 Neonoxites, 180, 1 80 Neopilina, 157 neoteny, 1 1 1 , 1 12, 1 1 2, 1 14, 1 1 7, 1 1 7 Nephrops, 214, 2 1 6 Nereis, 214 Nereites ichnofacies, 356, 358, 359, 359, 412 neurological control, flight, 76 Nevada, U . S . A . 481, 482 Newell's mass extinction events, 1 60, 1 6 1 niche, adaption to, 128, 141 -2, 146, 151 Nikon 'Multiphot' system, photography, 505, 506, 507 Nimbia, 18 Nimravus, 381 Niobrara Formation, Colorado, 410 nitrate, diagenesis, 213, 214, 216, 251 , 252 nitric acid, sample preparation, 504 nitric acid rain, extinction process, 165 nitrogen fixation, Precambrian, 49, 50 nodules, carbonates, diagenesis, 250 - 2, 251 , 252, 257 Lagerstatten, 2 73, 274 nomen nudum, AAP, 523 nomenclature, 425- 30 disarticulated animal fossils, 419-21,

Necro/emur,

420, 42 1

disarticulated plant fossils, 421 -3, 423 international Codes, 417-9 trace fossils, 423 - 5 'nonaptations', adaption, 145, 146 Nopsca, F., 543 Norian extinction, 40, 1 33, 1 73 , 1 74, 1 75 North American Cordillera, 487-8, 488 North China block, 187, 1 8 8 Norway, policy concerning status

material, 517 nostocalean cyanobacteria, 13 not polynomial-complete optimization problems, phylogenetic analysis, 497 nothosaurs extinction, 194 predation, 370 Nothrotileriops, 207, 208 notocacids, diversification, 50, 51

Notopocorystes slokesi, Notosaria, 1 15, 1 1 6

377

Notoungulata, extinction, 208

Nubeculinella,

348

nucleic acid, origin of life, 4, 6, 7, 8, 31 nucleotide sequences, 95 nucleus, eukaryotes, 30 nuculid bivalves, destruction of, 224 nutrients, extinction, 192 nutrition, terrestrialization, 65 Nye Klov, Denmark, 200, 201 , 202

Obruchevella, 26 obrution deposits, 239 - 43, 240, 242, 245, 268 -9, 269, 270 see also Hunsruck Slate Occam's razor, 454 ocean chemistry, Cambrian, 35 - 6, 35 ocean repository, origin of life, 3 - 7, 8 ocean tectonics, biostratigraphy, 484- 5 'oceanic anoxic events', 222 oceanic water circulation effect on diversification, 133 - 4, 192 extinction, 183-4, 1 83 octocorals, 25, 26, 3 2 , 33, 45, 48 Odaraia alata, 246 Ohmdenosaurus, 284 Oichnus, 369 oil, study of, 96 oil shale, 289, 290 Oldowan, tradition, 88, 89 18<x(H)-0Ieanane, biological marker, 219 Olenek uplift region, Siberia, 476, 477 'Olenellus Zone', 475 Olenoides, 273, 362 Oligocene angiosperms, 83 biogeography, 449, 450, 451 environmental indicators, 404, 404, 405, 41 1 , 412 grasslands, 84, 85, 86 Lagerstatten, 297, 297 molecular palaeontology, 98 palaeopathology, 381 predation, 370, 375 sea-level changes, 160, 161 size, 150, 151 oligochaetes, terrestrialization, 66, 68 oligohaline taxa, 407, 407 oncolites Precambrian, 10 stromatolites, 336, 337, 339, 340, 340 onychophorans, habitat, 65, 66 Onega, 20, 21 ontogenetic development evolutionary systematiCS, 435 heterochrony, 1 1 7 preservation, 292 trajectories, 431 , 498 Onverwacht Group, South Africa, 10, 1 1 , 12 oomycete fungi, terrestrialization, 63

574 Oort cloud of comets, extinction cause, 165, 177, 1 78 opaline skeletons, 24, 25, 27-8, 29, 314 Oparin, ocean scenario, 3 - 5, 7 Ophieeras Zone, Triassic, 1 88, 191 Ophiomorpha, 359 ophiuroids feeding, 389 Lagerstatten, 240, 242, 243, 283 opossum, Tertiary, 204 Oppel's use of zones, 461 opportunist species, 237- 8, 238 see also Burgess Shale; Hunsriick Slate; Solnhofen Limestone ophthalmosaurs, feeding, 363 optimality, experimental morphology, 308 - 9 Ordovician biofacies, 396, 396, 397, 398 -400 biomineralization, 26, 27 completeness of record, 299 diagenesis, 253-4 dietary evidence, 365, 366 diversification, 45, 46, 46, 47, 47, 132 encrusters, 347, 349, 3SO - 1 evolutionary fauna, 40 extinction, 37, 181 - 4, 1 8 1 , 1 83, 187, 194, 478 causes, 160, 161, 1 62, 1 67 Lagerstatten, 239, 240 microevolution, 108, 1 09 parasites, 378, 379 plankton, 51 , 52 predation, 370, 371, 3 71 reefs, 53, 54- 6 stratigraphy, 461, 468, 478- 80, 479, 483, 484, 485, 486, 486, 487, 488-91, 489, stromatolites, 336, 340 terrestrialization, 58, 58, 60, 6 1 taxonomy, 446 oreodonts, dentition, 86 organ genus, plant fossils, 422 organic acids, soil, 57 organic carbon decay processes, 213, 214 Precambrian, 49 source rocks, 220, 221 organic components, record of, 95- 6, 217-22, 2 1 8, 221 organic connection, plant fossils, 422 orientation, fossils, 227, 228, 244, 258, 259, 263, 286 origin of life, 3 - 9 conventional primitive ocean scenario, 3-7 alternative scenarios, 7 - 9 origination rate, species, 154-5, 156, 185, 186, 189 -90, 1 89 Oriskany Sandstone, Maryland, 224, 225 Ornithischia classification, 435, 436 defence, 375 herbivores, effect of angiosperms, 81 ornithomimids extinction, 205, 207 feeding, 363 ornithopod, extinction, 205 orogenic activity, extinction cause, 198 'Orsten' , Upper Cambrian, Sweden, 274 - 7, 2 75 Orthacea, extinction, 400 orthid brachiopods biofacies, 398, 399

Index extinction, 189 orthocones shells, 227, 229 orthogenesis, 126, 546, 547 Orthonota Mudstone, 395 'orthoselection', macroevolution, 126 orthostratigraphy, 461 Osborn, H . F . , 544, 546 oscillatoriacids, Archaean, SO, 51 osteichthyan fishes modern fauna, 38, 40 terrestrialization, 69 osteoarthritis, palaeopathology, 381 , 382, 383, 384 osteocalcin, skeletons, 317 osteolepiforms, terrestrialization, 69, 70 osteomyelitis, palaeopathology, 382 -3, 383 osteophytosis, palaeopathology, 382 osteoporosis, palaeopathology, 382 ostracodes biomineraliation, 25, 28, 29 biostratigraphy, 461, 468, 481 , 486 completeness of record, 299 environmental indicators, 406, 407 experimental morphology, 307 - 8 extinction 182, 1 83, 187, 189 hydrodynamics, 227 Lagerstatten, 276, 277, 279, 284, 292 leperditiid, 1 89 . Palaeozoic, 38, 40, 46 Ostrea ventilabrum 295 Otoeeras Zone, Triassic, 1 88, 191 Otozamites, 283 Ottoia, 364 outgroup analysis, 431 - 2 Ovatoscutum, 1 8 , 1 9 overpyrite diagenesis, 255 taphofacies, 259 Owen, R . , 545, 546 oxalic acid, lichens, 58 Oxford Clay, Wiltshire, 214, 2 1 5, 259 Oxroadia, 265 oxyaenids, predators, 375 oxygen levels amber concentration, 294 biofacies and trace fossil indicators, 356, 361 , 398, 409 decay processes, 213-4 diagenesis, 251 extinction cause, 199, 202 fossil concentrations, 237, 269, 270, 274, 283, 292, 293 molecular evidence, 219 Precambrian, 12, 1 3 - 14, 29, 548, 549 source rocks, 221 , 221 , 222 stromatolites, effect on, 337 taphofacies, 258 - 9, 259, 260, 261 , 262, 263 terrestrialization, 64- 5 oxygen isotopes, use of, 1 62, 1 67, 220 isotope ratios, environmental indicators, 403 - 5, 404, 405, 407- 8 oxygen-related ichnocoenosis (ORI), 410 Oxytoma, 283 oysters adaption, 142, 1 42 amino acids, 99 diagenesis, 247 encrusters, 346 heterochrony, 1 15 Lagerstatten, 267, 287

speciation, 108 Ozarkodina confluens, 421 Ozarkodina typica, 421

ozone layer extinction cause, 163 Vendian, SO

Pachycomus, 364 Pachycephalosaurus, 205, 207 Pachydiscus, 363 Pachypteris, 283 Pachytheca, 63 Pachytraga, 1 45

Pacific basin biogeography, 457, 458 paedomorphic processes, 108, 1 1 1 , 1 12, 1 1 2, 1 14, 1 15, 1 1 6, 1 1 6, 1 1 7, 1 18, 3 1 2 Pagiophyllum, 283 paiutiids, biomineralization, 25, 27 Palaemon, 214, 215 palaeoagraostology, 59, 83, 84- 7, 85, 87 palaeobiogeography, 484- 5, 549 palaeobiology, 551 - 2 Palaeobotryllus, 2 7 Palaeocene biogeography, 449 environmental indicators, 4 1 1 predation, 375 size, 150 Palaeochiropteryx tupaiodon, 291 palaeoclimate biogeography, use of, 458 biostratigraphy, 485 palaeocommunity, biofacies, 396 palaeocontinental distributions, 35 palaeoecology history of, 549, 550 trace fossils, 361 palaeoenvironmental classification, trace fossils, 425 Palaeofusulina Zone, 1 88 palaeogeography, 426, 452- 60, 452 , 453, 454, 455, 456, 457, 458, 459 palaeomagnetic signatures, use of, 438 Palaeopasciehn us, 180, 1 80 palaeopathology, 381 -4, 382, 383, 384 Palaeopleurosau rus, 284 palaeosols, evidence for grasslands, 85 Palaeospinax, 284 palaeotemperatures, 404- 5, 404, 405 Palaeotherium, 365 Palaeozoic coevolution, 137 diagenesis, 2SO dietary evidence, 363, 366 diversification, 37, 38- 9, 38, 39, 40, 41, 44, 45-6, 132, 133 environmental indicators, 404, 405, 405, 408, 412 encrusters, 347, 347, 349 heterochrony, 1 1 8 morphology, 307 parasites, 378, 379 predation, 370, 371, 3 71 , 373 problematic fossils, 443 plankton, 49, SO- 2, 51 size, 151 stratigraphy, 463, 467, 482, 484 taxonomy, 433 thermal maturity, 514 trophic structure, 386 Palaeozygopleura, 369 Palagosaurus, 284

Index Paleodictyon, 359 Paleoeriocoma, 84 PalielIa patelIiformis, 20 Palorchestidae, extinction, 208 palynological techniques, extraction procedures, 503, 504 palynomorphs, sample preparation, 502 503, 504 pampas, Oligocene, 85 Pangaea, 187, 188, 191, 192, 457, 484

Pan icum, 84 Panoplosaurus, 205, 207 Panthalassic ocean, biogeography, 457

Paracharnia, 21 parachuting/gliding theory flight, 74- 5 paradigm method, analogy, 143, 310 - 1 1 Paradise Creek, Australia, 53 Parahippus, 86 Parakidograptus acuminatus, 478, 479, 480 parallel evolution, 435, 546, 547, 551 biofacies, 398 paranotal lobes, flight, 72, 73 Paranthropus boisei, 88, 89 Paranthropus robustus, 88, 89 Paraorthograptus pacificus, 478, 479 parapatric speciation, 104 paraphyletic groups Cambrian, 39 cladistics, 428, 431 , 432 - 3 computer modelling, 497 diversity analYSiS, 447, 448 systematics, 436 taxonomy, 427, 428 Pararenicola, 30 parasitism, 136, 138, 376- 80, 3 77, 3 79, 385, 388, 390 parasitoids, 376 parastratigraphy, 461 parataxonomy, 419-20 Paratrilobita, classification, 22 Paris Basin, diagenesis, 257 Parka, 63 Parkinson, J . , (1755- 1824), 541 parsimony, 432, 434, 497 parthenogenesis, 102 particle size, source rocks, 221, 221 particulates, extinction cause, 178 Parvancorina, 21 pascichnia, trace fossils, 356 Passaloteuthis, 284, 284 passive feeding, suspension feeders, 43 pattern cladists, 429- 30, 431 - 2, 435 PaxielIa, 18, 20 pearls, formation, 378 - 9 peat formation, 352, 353, 354 peccaries, extinction, 208, 208 pecopterid ferns, extinction, 191 Pecopteris, 281 Pecten, 391 Pee Dee Formation, South Carolina (PDB), 403 Peking Man, 545 pelagic sediments, fossil record, 299 pelecosaurs, predators, 373 pelmatozoan echinoderms destruction of, 223 Palaeozoic, 54, 187, 189 Pelycosauria, paraphyletic groups, 433 penguins, biomechanics, 321 Penn Dixie Quarry, Blasdell, New York, 242 pennatulacean octocorals biomineralization, 26

Precambrian, 32, 33

Pentacrinites, 284

pentamerid brachiopods, biofacies, 399, 400 Pen tamerus, 391 , 395 Pentoxylon, 80, 81 peptides, molecular fossils, 97, 98 peramorphic processes, 1 1 1 , 1 1 2, 1 1 2, 1 14, 1 15, 1 1 6, 1 17, 1 18, 3 1 2 'perched faunas', extinction, 161 percoids, experimental morphology, 308 percussive techniques, preparation, 499- 500, 500 Pericosmus, 1 15 periodicity, extinction, 167, 171 - 8, 1 72, 1 73 , 1 74, 1 75, 194, 197, 553 periodontal disease, palaeopathology, 383, 3 84 periostracum, molluscs, 25 Peripatus, 65 Perischoechinoidea, paraphyletic groups, 433 Perisphinctes, 287 Perissodactyla, evolution rate, 153 'permanent varieties', 128 Permian biogeography, 458 dietary evidence, 363 diversification, 40, 47, 132 extinction, 160, 161, 1 62, 164, 167, 187-93, 187, 1 88, 1 89, 1 90, 373, 400 macroevolution processes, 131, 132, 133 Vendian, compared, 33 plant preservation, 264, 265 parasites, 378 predation, 373 size, 151 stratigraphy, 487-8, 488 stromatolites, 340 terrestrialization, 65 perrrlineralizations plants, 245, 263, 264 - 6, 264, 265, 352, 353, 354 skeletons, 224 see also mineralization Persimedusites, 18 Peru Upwelling, 222 Petalonamae, Precambrian, 18, 21 petioles, hydrodynamic properties of leaves, 230, 231, 232 petrifactions, plants, 263, 264 petroleum Lagerstatten, 289 molecular composition, 219, 220 petroleum source rocks, 408 petroporphyrins, chemical fossil, 96, 97 Peytoia nathorsti, 215 pH decay processes, 213 diagenesis, 251, 252 obrution deposits, 241 ocean, 163, 165 Phacops, 242, 278 phalanges, flight, 76 phalanx colonies, 334 phalanx strategy, encrusters, 347 'pharetronid' calcareous sponges, biomineralization, 26 phenetic biogeography, 437, 453- 4, 453 phenolic compounds, decay, 214 phenotype evolution rate, 1 53, 495, 497

575 origin of life, 6 - 7

Philippia krebsii, 455 Pholidophorus, 284, 366 phoronids, trace fossils of, 360

Phosphannulus, 378, 3 79

phosphate ocean chemistry, 35- 6 origin o f life, 8 soil, 57, 59 see also phosphatization phosphatization parasites, 378 skeletons, 27, 28, 28, 29, 44, 317, 379, 407 destruction of, 225 diagenesis, 245, 256- 7, 256 extraction techniques, 503-4 Lagerstatten, 267, 268, 273, 288, 291 'Orsten' depOSits, 274, 275 - 6, 277 phosphorite, stratigraphy, 476 photic zone, indicators of, 411 photo-oxidation, organic compounds, 217 photoautotrophs, Precambrian, 12, 14 photography, 505- 8, 506 Photomacroscop, photography, 505 photosynthesis bacteria, Cambrian, 27 grasses, 84 pigment, chemical fossil, 96, 97 Precambrian, 7, 12, 22, 50 stromatolites, evidence from, 336, 338 - 9 phragmocone, ammonites, 244, 244, 245 Phragmoteuthis, 284 phycocyanin, blue green algae, 49 Phycosiphon, 359 'phyletic rate', 154 phyletic transformation, 106, 107 phyllocarids, arthropods, 370 Phylloceratina, Triassic, 194 Phyllopod bed, British Columbia, 271 - 4, 272, 274 phylogenetics, analYSiS, 299, 425- 6, 428- 30, 434 see also cladistics; stratophenetic classification phylogeny, definition of, 434 physical environment, evolution effect on, 1 19, 121, 122 Stationary Model, 121 - 2, 1 2 1 Physoderoceras, 364 phytane, oxygen indicator, 219 phytoliths, grasslands, 84, 85 phytoplankton chemical composition, 96 extinction, 180, 185 Palaeozoic, 50, 51, 52 phytosaurs extinction, 194, 195 predators, 373 Picea pungens, 232 Piltdown fraud, 544 -5 pinnacle reefs, Palaeozoic, 56 Pinus succinifera, 294 Piptochaetium, 84 Pithecanthropus erectus, 88- 90, 89, 382, 544, 545 Pithonoton marginatum, 3 77 Placenticeras, 369 placer deposits, 269 placoderm fish extinction, 185, 194 Lagerstatten, 279 predation, 370 size, 148

Index

576 placodonts predation, 368, 370 teeth, 363 Placodus, 363 'Planet X', extinction, 178 plankton diversification, 49 - 52, 51 extinction, 121, 1 60, 1 63, 166, 183, 1 85, 199, 200 Red Queen Hypothesis, 136 see also nannoplankton planktotrophy, biogeography, 455, 455, 456, 456, 460 Planolites, 359 plants biomechanics, 319 coevolution, 137-8 communities, reconstruction of, 351 decay, 214 diagenesis, 254, 254 extinction, 1 63, 1 66, 187, 190, 1 90, 191, 1 97, 1 97, 203 -4, 204, 209 flattening, 245 galls, 378 preservation, 215, 263 - 6, 264, 265 Lagerstatten, 279, 281 , 283, 288, 292 size constraints, 147-9, 148, 151 source rocks, 220 terrestrialization, 60- 4, 6 1 thermal maturity, 514 transport-hydrodynamics, 230 -2, 231 see also angiosperms plastrons, biomechanics, 320 platanoid flowers, angiosperms, 80, 82 plate tectonics biostratigraphy, 484 - 6, 487 Cambrian, 36 development of, 547- 50 diversification, effect on, 133 - 4 eustasy, effect on, 1 62 habitat diversity, 42 Plateosaurus, 150 plattenkalks, 250, 252 -3, 285 Platygonus, 208, 208 platyhelminthes parasites, 377, 377, 378 - 9 Precambrian, 2 1 Platypholinia, 21 Platysuchus, 284 Plectospathodus flexuosus, 421 Pleistocene dietary evidence, 365, 367 extinction, 206-9, 208 grasslands, 84, 86, 87 Lagerstatten, 268 molecular palaeontology, 98 palaeopathology, 382 parasites, 377 predation, 375 - 6 reefs, 344 size, 151 stratigraphy, 468 pleopods, terrestrialization, 67 Plesiadapidae, stratophenetics, 439, 439 Plesiadapis, 440, 441 Plesiadapoidea, stratophenetics, 441 plesiomorphic state, 431 - 2, 435, 448 plesiosaurs biomechanics, 321 - 2, 322 extinction, 202 Lagerstatten, 284 predation, 363, 370 skeleton, 382

Plesiosaurus, 284

Plethodontidae, morphology, 3 1 2 , 313 Pliensbachian extinction, 1 73 , 1 74, 1 75 Pliocene grasslands, 85, 86, 87 molecular palaeontology, 98 predation, 376 size, 151 stratigraphy, 468 Pliohippus, 86 pliosaurids, feeding, 363 Podolia, Ukraine, U . S . S . R . , 481 , 482 podomere, arthropod, 319, 320 pogonophores feeding, 389 - 90 habitat, 64 Precambrian, 18 trace fossils, 360 poikilohydry, terrestrialization, 60, 64, 65 Poisson time series, 171, 1 72, 1 72, 1 73, 1 74, 1 75, 1 76, 1 77 Polecat Beach, Wyoming, 439, 439 Polinices aratus, 389, 389 Polinices duplicatus, 369 pollen biology, 82 - 3 evidence 79, 80, 80, 8 1 , 84, 88 diet, 354, 365, 367, 509 preservation, 264 thermal maturity, 5 1 1 , 512- 13, 513, 515 pollination coevolution, 138 hydrodynamics, 325 polyanionic constituents, origin of life, 8 polybutyl-methacrylate, sample preparation, 501 - 2 polychaete worms biofacies, 397, 400 encrusters, 346, 348, 358 feeding, 389 Lagerstatten, 271, 272, 279, 280, 281 polymeric agglutinations, fossil molecules, 96 Vendian, 44 polymerization, origin of life, 7 polymethyl methacrylate, sample preparation, SOl , S02 polymorphism colonies, 332, 333 population, 327- 8, 328 Polynices, 370 polypeptides, origin of life, 8, 31 polyphyletic group, taxonomy, 427, 432 polyploidy, reproductive isolation, 102, 1 02 polypyrimidines, origin of life, 6 polytypic species, 100 polyvinyl butyral resin, sample preparation, 501 Pomoria, 18 populations, 326- 29, 327, 328, 329, 329 genetic analysis, morphology, 313 structure, 23, 1 16, 151, 156 Porites, 343 porolepiforms, terrestrialization, 69 Poromya granulata, 390 porosity, sediments, effect on nodules, 2SO, 251 porphyrin, oxygen indicator, 2 1 8 , 219 Posidonia, 284 Posidonia Shales, Holzmaden, West Germany, 244, 270, 282 -4, 283, 284, 285, 364, 365, 395, 408

Posidonienschiefer, see Posidonia Shales post-displacement, heterochrony, 1 1 1 , 1 12, 1 1 2, 1 14, 1 1 7 postcranial skeletons, grazers, 86 postzygotic barriers, speciation, 101, 103 potassium hydroxide, sample preparation, 504 Pound Subgroup, South Australia, 1 7 Praecambridium, 2 1 Prague Basin, Czechoslovakia, 481 , 482 prairie, North America, 85 prasinophyte algae, Precambrian, 15, 50, 51 pre-displacement, heterochrony, I l l , 1 13, 1 13, 114 preadaptive hypothesis, adaption, 144, 145, 1 45, 146 Precambrian, 548 encrusters, 349 metazoans, 1 7 - 23, 19, 20 problematic fossils, 443, 444 prokaryotes and protists, 9 - 16, 1 4 reefs, 53, 53 soils, 57 stratigraphy, 470, 471, 474, 475-8, 477 terrestrialization, 57, 58 see also Archaean; Proterozoic precocious maturation, heterochrony, 1 12, 116 precoprolite, dietary evidence, 364 predation biomineralization, 29 bone transport, 233 Cambrian, 33, 34, 52 colonies, 334 computer analysis, 496 dietary evidence, 362 encrusters, 350 evolution, 1 19, 1 22, 136 - 7 heterochrony, 1 15 Lagerstatten, evidence, 288 marine, 368- 72, 369, 371 Mesozoic, 48 Precambrian, 18, 22, 23, 45, 50 size advantage, 151 skeletal damage, 223 terrestrial, 68, 373 - 6, 3 74 trace fossils, 357 trophic structure, 42, 385, 385, 386, 386, 386, 387, 388, 389, 390 premolars, hominids, 88 preparation chemical methods of, 500 - 1 , 501 macrofossils, 499 - 502, 500, 501 photography, 505 preservation processes, 268 preservational classification, trace fossils, 425 pressure force, hydrodynamics, 323 pressure, fossil molecules, 96 prey, coevolution, 136 - 7 prezygotic barriers, speciation, 101, 103 priapulids diversity, 426 habitat, 64 Lagerstatten, 271, 272 trace fossils, 360 Pffdoli Series, 480, 481 , 482 primates evolutionary diversification, 440, 441 speciation, 109 stratophenetics, 439, 439, 441 primitive ocean scenario, 3 - 7

Index Prins Karls Forland, Svalbard, 1 1 Prioniodus bicurvatus, 42 1

Priority, Principle of, 417, 418, 420, 422, 424 pristane, oxygen indicators, 219 Proarticulata, Precambrian, 21 probability, fossil record, 301 problematic fossil taxa, 442-4 LagersUitten, 271, 276, 2 80 Precambrian, 13 proboscideans extinction, 208, 208 Tertiary, 87, 208, 208 procolophonids, extinction, 194, 195 productid brachiopods biofacies, 400 extinction, 160, 189 Proeryon, 283, 284 progenesis, heterochrony, 1 1 1 , 1 12, 1 12, 114, 1 17, 1 1 7, 1 18 'progress', evolution, 120 - 1 progymnosperms concept of, 422 Palaeozoic, 40, 63 prokaryotes, Precambrian, 7, 10- 14, 1 1 , 15, 16, 30, 49 prolacertiforms, extinction, 194, 195 promotor region, heterochrony, 118 prosauropods, size, 150 Pro taster stellifer, 240 Protechiurus, 21 protein based life, S, 6 proteins decay, 217 molecular palaeontology, 95 skeletons, effect on, 317 Protenaster, 1 15, 1 1 6 proterochampsids, predators, 373 Proterozoic, 1 1 , 13- 16, 1 4 problematic fossils, 442, 447 stratigraphy, 461, 470, 471 -2, 474 stromatolites, 336, 337, 339, 339 proteutherian mammals, extinction, 204, 204 protists biomineralization, 24, 27 Precambrian, 10, 14, 15- 16, 50, 51 problematic taxa, 443 Protoarenicola, 30 proto-Atlantic, biostratigraphy, 485, 486 protoceratids dentition, 86 extinction, 205, 207 protoconodonts, Cambrian, 25, 28, 29, 34 protoctistans, Precambrian, 30 Protohertzina, 44, 45 Protohippus, 86 'protokerogen' , sediments, 217 protomammals, 373, 374 protopterygote insects, flight, 72, 74 Protostegidae, extinction, 205 Prototaxites, 6 1 , 63 proto-wings, flight, 72-5, 73, 78 protozoans parasitic, 380 terrestrialization, 65 provinces, diversity, 133, 134 provincialism, Precambrian, 18 prymnesiophyte algae, molecular composition, 220 pseudoextinction, 448 pseudo-Iebensspuren, trace fossils, 335 Pseudhipparion, 86

pseudomorphic textures, diagenesis, 255 Pseudomytiloides, 283 pseudopathology, 384 pseudopleochroism, diagenesis, 249 Pseudorotalia yabei, 5 1 0 pseudoscorpions, terrestrialization, 65 pseudotracheae, terrestrialization, 67 Psilonichnus ichnofacies, 356- 7, 358, 360 psilophytes, Lagerstatten, 279 Psilophyton, 63 Psocoptera, amber, 297 Pteranodon, 76 Pteridinium, 20, 21, 33 pteridophytes Cretaceous, 81, 83 Palaeozoic, 39, 40, 62, 64, 191 pteridosperrns extinction, 191 permineralization, 265 Pterocoma, 287 Pterodactyloidea, flight, 76 Pterodactylus, 287 Pterophyllum, 283 pteropods, environmental indicators, 412 pterosaurs biomechanics, 319 evolutionary faunas, 39, 41 flight, 75, 76, 77, 78 Lagerstatten, 284, 288, 289 predators, 375 size, 148 Triassic, 194, 195 pterygote insects biomechanics, 321 terrestrialization, 65 Ptychodus, 363 Ptycholepis, 284, 364 ptyctodonts, predators, 368, 370 Pulchrilamina, 54 pulmonates, terrestrialization, 65, 66, 67, 68 punctuated anagenesis, 108 punctuated equilibrium theory, 105, 107, 108, 109, 1 10, 127, 550, 552 computer analysis, 498 punctuationally derived species, 427, 428 Purbeck fossil forest, southern England, 264, 352 Purella, 34 purple bacteria, Precambrian, 16, 49 pycnoxylic wood, climate indicator, 402 pygostyle, birds, 78 pyrite decay product, 216 diagenesis, 245, 252, 253 -5, 254, 257 Lagerstatten, 241, 268, 269, 274, 282, 286, 291 Burgess Shale, 273, 2 73 Holzmaden, 282, 283 HunsrUck Slate, 277, 278 - 9, 278 plant preservation, 263, 264, 264, 266 specimens, storage, 515-6 surfaces, origin of life, 8 taphofacies, 259, 259, 260, 261 Pyrrophytes, Precambrian, 50, 51 Qasimia schysmae, 510 Q� virus, origin of life, 6 'quantum evolution', Simpson, 125, 127 quartz, extinction evidence, 163, 169, 1 69, 170 'quartz equivalents'

577 bones, 233, 234 shells, 228 quaternary diversification, 133 environmental indicators, 404 molecular palaeontology, 97 palaeopathology, 383, 384 reefs, 341 sea-level changes, 16 see also Holocene; Pleistocene quaternary 0, extraction techniques, 503 Quenstedtoceras lamberti Biozone, 466 Quetzalcoatlus, 76, 319

r-selection brackish environment, 407 heterochrony, 1 15, 1 1 7 Radiata, Precambrian, 18-20, 19, 20, 21, 23 radiation angiosperrns, 83 biomineralization, 26, 28, 29 community groups, 393 diversity analysis, 447- 8 encrusters, 347 Miocene, 376 Palaeozoic, 34, 36, 40, 46, 47 Precambrian, 23 see also evolutionary faunas radiolarians biomineralization, 25, 28 diagenesis, 256 environmental indicators, 412 geochronology, 483 Lagerstatten, 283 Palaeozoic, 50, 51, 52 preservation, 264 radiation, 185 Red Queen Hypothesis, 121, 1 23, 136 sample preparation, 502, 503, 504 speciation, 108 radiometric dating, u se of, 438, 461, 465 radula, gastropods, 362 Radulichnus, 351 Ramellina, 21 ramets, colonies, 331 , 332, 333, 334, 335 random processes, 109, 393 computer analysis, 495- 7 time series, 171, 1 72, 173, 1 74, 175, 1 75, 1 76, 177 Rangea, 21 rank, determination of, 51 1 - 5, 512, 513, 513, 514 Ranunculidae, Cretaceous, 81 Rassenkreis, speciation, 100 Rastrites maximus, 479 'rate hypomorphosis', heterochrony, 113 rates, evolution, 152-9, 156, 1 57, 1 58 Rawtheyan extinction see Ordovician Ray, J . , (1627- 1705), 539, 542 Raymond Quarry, British Columbia, 271 rays, feeding, 366, 368 recapitulation theory, 1 1 1 , 1 1 7, 545, 546 Recent see Holocene Receptaculita, 55 receptaculitid algae, Palaeozoic, 25, 54, 443 reciprocal overgrowth, encrusters, 348, 350 recruitment strategy encrusters, 346 populations, 326 recursion techniques, computer analysis, 495 red algae

Index

578 environmental indicators, 411 Ordovician, 54- 5 stromatolites, 336, 340 Red Queen Hypothesis, 1 1 9 - 24, 1 20, 1 2 2 , 1 23 , 129, 136, 550, 553, 554 Redkil1ia spil1osa, 22 redox potential discontinuity (RPD), 241 redox process, 8, 42 reefs, 52- 6, 53 , 55 biofacies, 398, 400 carbonate build-ups, 341 - 5, 342, 343, 344, 393 -4 colonies, 330 communities, 393 -4 encrusters, 349 extinction, 1 60, 1 67, 184, 185, 189 heterochrony, 1 1 7 Solnhofen Limestones, 286 stromatolites, 340 see also Burgess Shale reflectivity, vitrinite, 511 -2, 5 1 2 , 5 1 3 , 513, 514, 515 refractories, decay process 214, 254 'regulatory genes' , heterochrony, 1 1 8 regurgitates, dietary evidence, 364 Relzbachiella kil1l1ekullel1sis, 276 reinforcement, microevolution, 103 ReIlalcis, 54, 56 repichnia, trace fossils, 355 replacement ratio, extinction events, 18990 replica tor, selection, 127 reproduction angiosperms, 81 barriers, 198 biogeography, 455 colonies, 331 - 2, 335 heterochrony, 1 1 5 hierarchy theory, 126 isolation, 100 - 6, 1 02 , 132 Radiata, 18 size advantage, 151 terrestrialization, 68, 70 reptiles biomechanics, 321 - 2, 322 classification, 433, 435 - 6, 436 dentition, 363, 363 evolutionary faunas, 38, 39, 41 extinction, 190, 1 90, 194, 195, 1 95, 196, 204 - 5, 205, 206, 207, 207 Lagerstatten, 284, 288 paraphyletic group, 432, 433 predators, 370, 373, 374, 3 74, 375, 363, 370 skeleton, 382 size, 148 terrestrialization, 68, 70 see also dinosaurs; plesiosaurs; pterosaurs; synapsid reptiles; therapsid reptiles resins Baltic amber, 294 - 7, 294, 295, 296, 297 preservation, 268 resource specialization, 156, 157 tracking, 138 respiration mineralized skeletons, 29 size constraints, 149 terrestrialization, 67, 69 resting traces, trace fossils, 355 Relusa kel/ogii, 389 reversal, evolution, 109- 10, 435

Reynolds number, 320, 321, 323 - 4, 325 rhabdosomal stabilisers, graptolites, 52 Rhaetian extinction, 1 73 , 1 74, 1 75 Rhamphorhynchoidea, 76 'Rhinean' , sediments, West Germany, 277 rhinoceros dentition, 86 Lagerstatten, 268 size advantage, 151 Rhipidistia, paraphyletic groups, 433

Rhipido11lella, 369 Rhizocoralliu11l, 359, 365 rhizomes, grasses, 84 rhizopods, modern fauna, 38, 48 rhizosphere, terrestrialization, 59, 64 Rizizosto11liles, 287 Rhodesian Man, 383

Rlzododendron,

231

rhodoliths, environmental indicators, 411 rhyncholites, cephalopods, 370 rhynchosaurs, extinction, 194, 195, 1 95 Rhynchota, Baltic amber, 297, 297 Rhynia, 62, 137 Rhynie Chert, Aberdeen coevolution, 137 plant preservation, 264 permineralization, 352 terres trializa tion evidence, 58, 59, 63, 64, 65, 68 rhyniophytoid, terrestrialization, 6 1 , 62 rhynchonellid brachiopods, biofacies, 400 Riftin pachypliln, 389 rifting Cambrian, 35 Grube Messel, 290 Riphean, plankton, 50, 51 RNA genetic analysis, 327 metazoan evolution, 31 origin of life, 6, 7 respiration evidence, 14 robust patterns, stratophenetics, 438, 439 440 Roclzdalia parkeri, 73 rodents caviomorph, 208 evolution rate, 153 feeding, 367 prey, 376 size, 1 5 1

Rogerella,

360

Ronner, F., 469 'roof shale' floras, 353 root-traces, grassland soils, 84, 85 rooted soils, terrestrialization, 58, 59 rosid dicotyledons, Cretaceous, 81

Rosselia,

359

rotifers and acanthocephalans, 377 terrestrialization, 65 rudist bivalves extinction, 201, 400 preadaptive hypothesis, 144, 1 45 reefs, 342 size, 151 Rugocol1ites, 18 rugophilic behaviour, encrusters, 349 rugose corals encrusters, 347 extinction, 160, 184-5, 187, 189 Ordovician , 54, 55 ruminants, Tertiary, 87

runner form, encrusters, 347, 347, 350 running/jumping theory, flight, 74, 78 Rusicizllites grenvillel1sis, 424 Russian Platform, 17, 180, 182, 187 rhyncholites, cephalopods, 370 sabelliditids, Cambrian, 22, 54 sabre toothed cats extinction, 207, 208, 208 palaeopathology, 381 predators, 151, 375 - 6 Snccoco11la, 287, 288, 364 safety factor analysis, experimental morphology, 309

Sagel1el/a,

348

salamanders heterochrony, 1 16, 1 1 8 Lagerstatten, 292 morphology, 3 1 2 , 313 terrestrialization, 69 saleniid echinoids, heterochrony, 1 14 salinity biofacies, 398 diagenesis, 247, 255 extinction cause, 191, 199 fossil concentrations, 237, 241 , 242, 286, 287, 288 indicators, 406- 8, 407 molecular evidence, 219, 22 1 , 222 stromatolites, 337 trace fossils, 356, 357, 361 Salopel/a, 62 Salopella -like sporangia, 60, 62 Salpil1goleullzis, 284 salps, colonies, 330, 334 saltation theory, macroevolution, 124 Salvil1ia, 367 Samland Promontory, U . S . S . R . , Baltic amber, 294 - 7, 294, 295, 296, 297 sample size, fossil record, 301 sampling model, 446, 447 San Andreas Fault, North America, 486 sandstones, extraction techniques, 503 sanidine, extinction evidence, 169 Santana Formation, Brazil, Cretaceous, 277 sapropel, Vendian, 180 satellite taxa, nomenclature, 423 saurischian dinosaurs, predation, 374 - 5 sauropods feeding, 363, 364, 375 size, 151 sauropsids terrestrialization, 68 see also birds; mammals Saurorhyl1clzus, 284 savanna, spread of, 85, 86, 138 scaffolds, skeletons, 314 scallops diagenesis, 247 molecular remnants, 97, 98 scanning electron microscopy (SEM), 505, 5 1 0 , 509 - 1 1 scanstore, electron microscopy, 5 1 1 scavengers Cambrian, 33 definition of, 213 destructive processes, 223 Lagerstatten, 288 Precambrian, 18, 22, 23 shell hydrodynamics, 229, 233 trace fossils, 357, 359 trophic structure, 385, 386, 388

Index Scelidosaurus harrisoni, 501 Scheuchzer, J . , (1672 - 1 733), 539 Schizaster, 1 1 5 schizogenic mode, resin production, 295 Schizoporella, 348 'schlauben', resin, 295 - 6, 296 Schuchert, c . , 547 sciotaxon, definition of, 421 scleractinian corals biomineralization, 26 encrusters, 347 Triassic, 189 sclerites Precambrian - Cambrian, 22, 24, 27, 34, 44, 45, 443 sclerocytes, biomineralization, 26 sclerosponges biomineralization, 26 problematica, 443 scolecodonts, sample preparation, 502 scorpions Lagerstatten, 279 terrestrialization, 65, 66, 67 Scoyenia ichnofacies, 356, 358, 4 1 2 scrapers, effect on reefs, 56 Scrobicularia, 389 Scyliorhinus, 366 Scyphozoa Lagerstatten, 282, 286, 287, 288 Precambrian, 18, 21, 32, 44 sea-level biases in fossil record, 130 biostratigraphy, 488 - 90, 489 changes, reefs, 344- 5 extinction process, 160-2, 1 61 , 163, 164, 166 events, 182 - 3, 1 83, 184, 187, 188, 192, 193, 199, 197 source rocks, 220 variations, Palaeozoic, 35, 35, 42, 478, 479 sea-lions biomechanics, 321 - 2 predation, 370 seals, predation, 370 seasonality, extinction, 187, 188, 193, 203 -4 seaweeds see algae 'secondary adaption', 145 sediment grain size, trace fossils, 361 sedimentary record completeness of, 298 -9, 298 extinction evidence, 169 sedimentation rate completeness of fossil record, 298, 298, 299, 301 , 302 fossil concentrations, 236, 236, 237 Lagerstatten, 240, 243, 267, 277, 281, 282, 291 source rocks, 221 , 221 taphofacies, 258, 258, 259, 259, 260, 260, 261 , 261, 262, 263 trace fossils, 356, 362 seeds angiosperms, 79, 83 hydrodynamics, 231 segmentation, Coelenterata, 21, 23 Seirocrinus, 284 seismic stratigraphy, 471, 472 selectivity, extinction, 167 semicircular canals, terrestrialization, 70 sense organs skeleton, 314

terrestrialization, 65, 68, 70 septaria, nodules, 251, 251 sequence stratigraphy, 302, 302, 359, 472 sequestrants, sample preparation, 500 Sequoia, 151 serpulids, encrusters, 347, 350 settling, shells, 227-8, 228 sexual dimorphism, hominids, 88, 89 sexual selection, macroevolution, 126, 127 sharks feeding, 363, 364, 365, 366 Lagerstatten, 284, 288 predation, 368, 369, 370, 371 shear force, hydrodynamics, 323 sheep, teeth, 234 sheet form, encrusters, 347, 347, 350 shells Cambrian, 24 -9, 25, 28 composition, 314 diagenesis, 254 flattening, 244 hydrodynamics, 227- 9, 228, 229 morphology, 3 1 1 predation, 368, 369, 3 6 9 , 370, 3 7 1 , 372 taphofacies, 258, 259 shock-metamorphosed minerals, extinction evidence, 163, 169, 1 69, 1 70, 1 77, 198 shrimp, Lagerstatten, 282, 292 Siberian traps, associated, extinction, 1 78 sibling species, speciation, 100 Sichuan, China, 169 siderite coprolites, 366 Lagerstatten, 241, 291, 292 concretions Mazon Creek, 279, 281 - 2, 282 nodules, 250, 251, 252 Sidneyia, 362, 364 Signor-Lipps effect, 166 silica coprolites, 366 fossils, Cambrian, 27-8, 28, 34 plants, 84, 138, 263, 264, 264 stability, 225 Silurian biofacies, 395, 397, 397, 398 - 400 biomineralization, 26 communities, 391, 392 completeness of record, 299 diversification, 46 - 7 evolutionary flora, 40 environmental indicators, 411, 412 Lagerstatten, 26/ parasites, 378-9, 380 plankton, 51 , 52 predation, 371, 372, 373 reefs, 53, 55 -6, 345 stratigraphy, 461, 463, 465, 466, 468, 475, 478 - 82, 479, 481 , 483, 488, 489 terrestrialization, 58, 59, 60, 6 1 , 62, 63, 64, 65, 67, 68 similarity coefficients, phenetic biogeography, 453 -4, 453 Simpson, G . G . , 546, 547 Simpson similarity coefficient, 453, 454, 454 'Simpsonian systematics', 434 simulation modelling, 493 - 4, 494, 496 Sinan thropus, 545 Sinian, 17 see also Vendian Sillosabellidites, 30

579 siphogonuchitids, Cambrian, 34 siphonophores colonies, 330, 332, 333, 334 Lagerstatten, 279 sipunculids habitat, 64 trace fossils, 360 sister-groups, 430, 433, 435, 437, 448 size destructive processes, 224, 226 evolution, 108, 137, 147-52, 148, 149, 1 50, 151 extinction, 161 flight, 76 heterochrony, 1 12, 1 1 3, 1 15, 1 16, 1 1 7 leaves, transport, 230, 231 Palaeozoic, 45, 47 Precambrian, 18, 22, 23 terrestrialization, 76 Skara, 275, 276 skeletons biases in fossil record, 130 Skaracarida, Lagerstatten, 276 composition and growth, 314- 18, 315, 316 encrusters, 346 experimental morphology, 307 palaeopathology, 381 - 4, 382, 384, 385 Precambrian- Cambrian, 22, 24 - 9, 25, 28, 33, 34, 36, 45 vertebrates, heterogeny, 1 1 8 Skiagia, 180 skins, Tertiary, 205 Skillnera, 18 skolithid reefs, 54 Skolit/ws, 45 ichnofacies, 356, 357, 358, 359, 360, 361 , 412, 4 1 2 skull hominids, 88, 89, 90, 91 mammals, 145 Slave Province, Canada, reef formation, 53 sloths extinction, 208, 208 feeding, 367 preservation, Lagerstatten, 268 size, 150 'small shelly faunas', Cambrian, 39 smectite, Lagerstatten, 291 Smilodol1, 207, 2U8 Smith, W . , ( 1 769 - 1839), 541 , 54 1 , 542 Smittina exertaviculata, 332 snails, terrestrialization, 65 snakes Cretaceous, 205 Lagerstatten, 292 predators, 376 Snowdon, 490 soaring, flight, 75, 76 societies and organisations, 522 -4, 530 sodium hexametaphosphate, sample preparation, 500 sodium hypochlorite, extraction techniques, 503 sodium polytungstate, concentration techniques, 504 sodium thiosulphate, extraction techniques, 503 soft parts decay, 213, 214, 215 diagenesis, 253, 254, 257 encrusters, 346, 350 flattening, 245

580 fossil concentrations, 237, 276, 277 Grube Messel, 292, 293 Holzmaden, 283, 284 Solnhofen, 287, 288 fossil record, effect on, 389, 426, 445 parasites, 377, 380 trace fossils, 180, 356, 357, 360 soils, terrestrialization, 57-9 solar heat output, extinction, 164 Solar System see extra-terrestrial cause Solemya, 283 solemyid bivalves, trophic structure, 390 Solenopora, 54 solitary encrusters, 346, 347, 347, 350 Solnhofen Limestone, West Germany, 239, 240, 244, 268, 269, 270, 285- 9, 286, 287, 289 Archaeopteryx, 78, 288, 289, 543 diagenesis, 253 dietary evidence, 364 soot, extinction evidence, 169 Sorenson similarity coefficient, 453, 454 source rocks, 220-2, 221 South China block, 187, 1 88 Southern Uplands, Scotland, 483 space competition, benthic habitat, 42, 43 spatangoid echinoids, heterochrony, 115 Spathodus prim u s , 421 spa tial refuges colonies, 334 encrusters, 347 speciation, 100 -6, 1 02, 107 angiosperms, 82 heterochrony, 114 hierarchies, 125 - 6 rate, 156 - 7, 158, 159, 198 study of, 299, 548, 552, 553 Vendian, 22 species definition, 100, 107 diversity, 1 34, 445 - 7, 446 extinction, 185, 186, 1 86 immunological techniques, 99 selection, 127, 552-3 species - area effect, 192 'specific mate recognition system (SMRS)" 126 Sphaerirhynchia (Wilsonia) wilsoni, 395 sphalerite, Lagerstatten, 281 Sphenacodontidae, predators, 373 Sphenodon, 157 sphenodontid, Lagerstatten, 284 sphenopsids, Palaeozoic, 40, 63 spheroids, Precambrian, 10, 1 1 , 12, 14 spherules, extinction evidence, 169, 170 spherulites, skeletons, 315, 315, 316- 1 7, 316 sphinctozoans, biomineralization, 26 spicular skeleton, Precambrian­ Cambrian, 24, 26, 27, 28, 33 spicules, problematic taxa, 443 spiders Lagerstatten, 279, 292 predators, 373 terrestrialization, 59, 65 spinosity, prey, 371 , 372 spirorbids, symbiotic, 138 Spirophyton, 359 Spirorbis, 348 Spirorhaphe, 359 Spitsbergen, Triassic, 277 Spongeliomorpha, 360 sponges

Index clinoid, 224, 225 coloniality, 330, 333 coralline, 443 durability, 224, 225 encrusters, 346, 347, 348, 350 extinction, 184, 185, 194 hexactinellid, 26, 28 Lagerstatten, 271, 2 72, 273, 273, 292 lithistid, 54 modern, 38, 48 Palaeozoic, 45, 46, 52, 53, 54 Cambrian, 23, 26, 34, 45 problematic taxa, 443 reefs, 342, 343 skeleton, 26, 27, 28, 314, 315 trace fossils, 360 Spore Colour Index (SCI), 512, 5 1 3 spores biostratigraphy, 461, 467 electron microscopy, 509 preservation, 264 terrestrialization, 60, 62, 63 thermal maturity, 511, 512 - 1 3, 513, 513, 514, 515 sporomorphs, terrestrialization, 60 -2, 6 1 sporopoUenin, terrestrialization, 60 Spriggina, 21 Sprigginidae, Precambrian, 21 - 2 springtails, terrestrialization, 58, 59 Squamata classification, 435, 436 extinction, 205, 206 squids, 287 stable isotopes, use of, 35, 35, 251, 252 stagnation deposits, 239, 268- 70, 269, 283 see also Burgess Shale; Grube Messel; Hunsriick Slate; Solnhofen Limestone stamen, angiosperms, 80 stand-off, encrusters, 350 standard mean ocean water (SMOW), 403 stapes, terrestrial vertebrates, 70 starch grains, preservation, 264 starfish see asteroids stasis, 107, 108, 109, 110, 124, 125, 552 Stationary Model, evolution, 121 -2, 1 2 1 status material, storage, 516 - 7 S taurinidia, 18 stearate, diagenesis, 252 Steganotheca, 62 Stegoceros, 205, 207 stegosaurs defence, 375 feeding, 363, 364 Steinheim, West Germany, 90 steinkern pyrite, taphofacies, 259, 259, 261 Steinmannia, 284 stellate microfossils, Precambrian, 13 stelleroids, Palaeozoic, 38, 46 stem-group, classification, 433, 437 Steinmannia, 284 Stenodictya, 73 stenohaline taxa, environmental indicators, 406 stenolaemate bryozoans, diversification, 38, 46, 347 Stenomyelon tuedianum, 265 Stenopterygius, 284, 285, 285 stenotopic species, speciation and extinction, 123, 158, 162 Stensen, N" ( 1638 - 1 686 ) , 538 Stephen Formation, British Columbia, see Burgess Shale

stereological techniques, 301 stereom, echinoderms, 26, 62, 315- 16, 318 stereophotography, 508 sterile axes, Devonian, 62 sterility, reproductive isolation, 102 sterna, flight, 77, 78 steroids, information from, 218 Stevns Klint, Denmark, 201 Stigmaria, 423 Stipa, 84 S tipidium, 84 stomach contents, evidence of diet, 363 stomata, leaves, 60, 62, 231, 402 stomatopods, predators and prey, 368, 370, 372 Stone City Formation, southeast Texas, 389 storage, specimens, 515- 7 storms extinction, 188 fossil concentrations, 236, 237, 240, 267, 283 Solnhofen Limestone, 286, 288, 289 taphofacies, 258, 261 stratiform conservation deposits, 268 stratiform stromatolites, 336, 338, 339, 340 stratigraphy analysis, 30, 155 - 6, 429, 430, 437 biofacies, 395 -6, 3 95 range, completeness of record, 301 - 2, 3 02 stratigraphy and stratophenetics, 437, 438, 439, 439 stratophenetic classification, 427, 429, 435, 437-41, 439, 440, 551 computer modelling, 497 strength, biomechanical study, 318-20, 319 Stricklandian Code, 417, 418 stridulatory organs, terrestrialization, 68 Striispirifer, 240 stroma, biomechanics, 318 stromatactis, reefs, 54, 55, 56 stromatolites, 336- 40, 336, 337, 338, 339, 340, 548 Cambrian, 35, 54 columnar, 336, 336, 337, 337, 338, 339, 399 , 340 domical, 336, 337, 337, 338, 338, 339, 340 IGCP project, 470 Lagerstatten, 286 metazoans and, 179, 339, 340 origin of life, 7 Precambrian, 10, 1 1 , 12, 13, 14, 15, 17, 31, 49, 51 reefs, 53, 53, 54, 55, 56 stratiform, 336, 338, 339, 340 stratigraphy, 476 stromatoporoids, 346 encrusters, substrate for, 349 environmental indicators, 411 extinction, 168, 1 79, 182, 184, 185 hydrodynamics, 325 problematic taxa, 443 reefs, 341, 342 , 344 symbiotic, 138 strontium aragonite, 247, 249 salinity indicator, 407 strophomenid brachiopods biofacies, 399 extinction, 194 'structural genes', heterochrony, 118

Index Stygimoloch, 205, 207 subduction zones, Cambrian, 36 subholosteans, Lagerstatten, 284 subjugation, predation, 368 substrate biofacies, 398 trace fossils, 357, 359 - 60, 361 sulphate diagenesis, 251 , 252, 252 , 253, 254, 254, 255 extinction, 178 Precambrian- Cambrian, 12, 13, 15, 35, 35 reduction decay process, 213, 216 Lagerstatten, 240, 240, 281 , 282 sulphide oxidizing bacteria, 390, 390, 409 sulphidic environments, pyrite formation, 261 'superorganisms', colonies, 335 support, terrestrialization, 65, 70 surface tension, biomechanics, 320 survivorship curves, 389, 389 suspension feeding, 18, 22, 23, 38 bivalves, 399, 400 encrusters, 346 Lagerstatten, 276 tiering structure, 41, 42, 43-4, 44, 45, 45, 46, 46, 47, 48 trace fossils, 356, 357, 360 trophic structure, 385, 385, 386, 386, 386, 387, 388, 389 Swanscombe, England, 90 Swartkrans, South Africa, 88 Swedish Caledonides, biostratigraphy, 484 swimming, biomechanics, 321 symbiosis, 376, 377, 380, 389 - 90, 390 taxa, coevolution, 136, 138 terrestrialization, 59, 63 symmetry anabaritids, 24 Coelenterata, 23 shells, 227 Symmorium, 371 sympatric speciation, 104 symplesiomorphies, 430 - 1 , 43 1 , 432 synapomorphies, 126, 430, 431, 431 , 432, 433 synapsid reptiles classification, 436 evolutionary faunas, 39, 41 predators, 373 syneresis, Lagerstatten, 282, 287 syntaxial cement precipitation, diagenesis, 250 syringoporids, Ordovician, 55 systematics, 18 -22, 549

Tabulaconus, 26 tabulate corals Palaeozoic, 25, 54, 55, 182, 187, 189, 347 problematic taxa, 443 'tachytely', evolution rate, 153, 1 58 taiga, Post-Pleistocene, 84 talitrids, amphipods, terrestrialization, 67, 68 talus blocks, reefs, 56, 343 -4 Tamaulipas, Mexico, 367 Tan nuolina, 27 taphocoenosis, 237, 238, 238, 258 taphofacies, 258 -62, 258, 259, 260, 2 6 1 , 2 6 2 , 263

taphonomic facies see taphofacies taphonomy environmental indicators, 412 processes, 223 -6, 224, 225, 226 obrution deposits, 243 plants, 352 - 3 trace fossils, 360 tapirs, dentition, 86 tardigrades, terrestrialization, 65 Tarsioidea, 440, 441 Tasmanites, 50, 51 Tawuia, 30

taxonomy composition, compared fossil concentration, 235, 236 diversity, 131 -3, 1 3 1 , 132, 447, 553 evolution, 153, 154, 155, 156 journals, 524 teaching, exhibit strategies, 519- 22, 521 tectonics, 482- 90, 486, 487, 488, 489 biogeography, 454 - 5, 457, 458, 458 extinction, 1 62, 191, 192, 193 preservation, 274 teeth hominids, 88, 89, 90, 91 shells, 227 palaeopathology, 381, 383 predators, 373 transport, 233, 234 vertebrates, 362-3, 363, 364 Tegulorhynchia, 1 15, 1 1 6 Teichichnus, 359 teids, Tertiary, 205, 206 teleology, adaption, 139, 140, 144, 145 teleostean fishes biogeography, 449, 450, 450, 451 Lagerstatten, 284, 287 Tel/ina, 389 Tellinacea Mesozoic, 400 trophic structure, 389 temnospondyl amphibians, terrestrialization, 70 temperature biogeography, 457 decay processes, 213, 214 dependent organisms, 412 diagenesis, 247 extinction events, 183, 1 83, 184, 185, 198, 199 Permian, 187, 188, 1 88, 191, 192 extinction process, 161, 162, 1 63, 165, 166, 167 heterochrony, 1 1 6 hydrodynamics, 323 obrution deposits, 241 , 242 oceans, molecular evidence, 96 oxygen isotope ratios, use of, 403 - 5, 404, 405 plant indicators, 401, 401 , 402, 402, 403 Precambrian, 12 specimen storage, 515, 516 source rocks, 219, 220, 221 stromatolites, 337 trace fossils, 357, 360 see also thermal maturity templating, origin of life, 5, 6, tentaculites biomineralization, 25 problematic taxa, 442, 443 shells, 229 terabratulid brachiopods, biofacies, 400 Tcredo/itcs, 425

581 ichnofacies, 356, 358, 359, 360 terrestrial (earth-bound) cause, extinction, 171, 172, 1 77, 1 78 Cretaceous - Tertiary, 203 -5, 204, 205, 206, 207 terrestrial environment, diversity of species, 130, 132, 132, 133, 134 predators, 373 -6, 3 74 terrestrialization invertebrates, 64- 8, 65 plants, 40, 60 -4, 61 soils, 57-9, 58 vertebrates, 40 - 1 , 68 - 72, 69, 71 Tertiary angiosperms, 82 - 3 biofacies, 400 biogeography, 455, 456, 456 diagenesis, 257 diversification, 132, 1 32, 134 environmental indicators, 404, 412 grasslands, 84- 5, 86, 87 heterochrony, 1 15, 1 1 7, 1 18 Lagerstatten, 268 microevolution, 109 nomenclature, 422 plant communities, 352, 354 preservation, 266 predation, 370, 375, 376 reefs, 344 size, 151 stratigraphy, 461, 484 see also Baltic amber; Grube Messel Testudinata, classification, 435, 436 Tethys Ocean, 286 tetrabromoethane, concentration techniques, 504 Tetradium, 55 tetrads, Palaeozoic cryptospores, 60, 61 Tetragonolepis, 284 Tetramatosau nts, 284 tetra ploidy , reproductive isolation, 102, 1 02 tetrapods, 68- 71 , 69, 7I choana, 69 diphyletic, 69 experimental morphology, 307, 308 extinction, 190 - 1 , 1 90, 192, 194, 195, 196, 197, 1 97, 198 Lagerstatten, 279 Palaeozoic, 39, 40- 1, 68 -71, 69, 7I predators, 373 - 6, 374 Teudopsis, 284 TIlalassinoides, 47, 359, 366 Thallophyta, Palaeozoic, 60, 64 thanatocoenosis, 237, 238, 258, 268, 276 Tharsis dubius, 287 Thaumatosaurus, 284 thecideidine brachiopods, heterochrony, 1 14 thecodontians classification, 436 extinction, 194, 195, 1 95 predators, 373, 374 Thecodontosaurus, 1 97 theoretical morphology, 310, 311 theoretical palaeobiology, 551 , 552 Therapoda, classification, 436, 436 therapsid reptiles classification, 443, 436, 436 cynodont, 151, 373, 374 extinction, 190, 1 90 predators, 373, 374, 3 74, 375

582 terrestrialization, 68

Index

obrution deposits, 239, 240 preservation, effect on, 214-5, 2 1 6, 223 Thermal Alteration Index (TAl), 513 tree ferns, Carboniferous, 354 thermal maturity, determination of, tree rings, climate indicator, 402 51 1 - 5, 512, 513, 513, 514 trematodes, parasites, 377, 378 thermophilic conditions, Precambrian, 7, trepostome bryozoans, extinction, 1 60, 189 12 Triarthrus, 240 thermoregulation, pro-wings, 72 Trilobite Bed, New York, 253- 4 theropod dinosaurs Triassic bird ancestors, 1 14 angiosperms, 79, 81 predators, 374 biofacies, 400 Tlzescelosaurus, 205, 207 biogeography, 457, 458 Theta- rho analysis, 31 1 - 12 coevolution rate, 137 TllOracosplzaera, 201 dietary evidence, 366 thrombolites, stromatolites, 336, 339, 340 diversification, 132 thyasirid bivalves, trophic structure, 390 evolution rate, 157 Thylacoleonidae, extinction, 208 evolutionary fauna, 40, 41 tiarechinid echinoids, heterochrony, 1 14 extinction, 194 - 8, 1 95, 1 96, 197 tiering, 38, 42, 43 - 4, 44, 45-8, 45, 46, 47, causes, 1 60, 161, 167, 189 133 flight, 76 marine habitat, 46-8 Lagerstatten, 269 Tilestones, South Wales, 480 plant preservation, 264 time averaging, fossil concentrations, predation 372, 373 - 4, 374 237-8, 238 size, 150 'time hypomorphosis', heterochrony, 1 1 3 stratigraphy, 488 Tirasiana, 1 8 Tribraclzidium, 18 Tithonian extinction, 1 73 , 1 74, 1 75 Triceratops, 205, 207, 375 Tomaculum, coprolites, 366 trichobothria, ttrrestrialization, 68 Tommotian Fauna, 39, 40, 44- 5 TricilOdesmium, 49, 50 tommotiids, Cambrian, 25, 27, 34 Triclzognatlzus symmetrica, 421 tools, hominids, 88, 89 - 90, 89, 91 Trichoptera, Baltic amber, 297, 297 Tornquist's Sea, biostratigraphy, 485, 486 tricolpate pollen, Cretaceous, 80, 81 Torosaurus, 205, 207 tricolporate pollen, Cretaceous, 81 total-range biozone, 461 tridactyl feet, horses, 86 trabeculae, coral skeletons, 26 trigonotarbid arachnids, terrestrialization, trace elements 59, 65 extinction cause, 165, 191 trilobites shells, salinity indicators, 407 biofacies, 396, 398, 399 trace fossils, 355 - 62, 355, 357, 358, 359, biostratigraphy, 461 , 462, 475, 477, 485, 360, 549 486 diet evidence, 362 completeness of fossil record, 302 diversity, 1 34, 180 diagenesis, 250, 253- 4 durability, 224 extinction, 1 60, 181, 1 8 1 , 182, 1 83 , 189 environmental indicators, 409 - 10, 4 1 0, feeding, 362 4 1 1 , 412, 412 flattening, 245, 246 Lagerstatten, 277, 282 galls, 379- 80 modern, 48 heterochrony, 1 14, 1 15, 1 17, 1 1 8 Lagerstatten, 239, 240 - 1 , 240, 242, 243, nomenclature, 423- 5 Palaeozoic, 34- 5, 44, 45, 47 267, 269 parasites, 378 Burgess Shale, 271, 272, 273, 273 'Orsten' deposits, 274, 276 Precambrian, 10, 33, 49 lineages, 428 predation, 368 Palaeozoic, 26, 34, 38, 44, 45, 52, 54, 480 stratigraphy, 476, 477, 478 parasites of, 379- 80 see also oncolites; stromatolites photography, 506 tracheae, terrestrialization, 67, 72, 73, 142 Precambrian, 21 tracheophytes speciation, 107, 108, 1 09 diversity of species, 130, 132 - 3, 1 32, 134 taphofacies, 259, 260 Palaeozoic, 39, 40, 58, 59, 60, 6 1 , 62, 63, terrestrialization, 65, 67 64 Trilobozoa, Precambrian, 18, 21 Traclzymetopon, 284 trimerophytes, Palaeozoic, 63, 64 Traclzysplzaeridium laufeldi, 1 79 Trionyx messelianus, 290 transformation approach to morphology, trophic structure, 191, 193, 385 - 90, 385, 309 - 10, 3 1 0 386, 386, 387, 388, 389, 390 transformation cladistics, 429 - 30, 431 - 2, tropical ecosystems 435 extinction, 189 transmission electron microscopy, 508 -9, forests, Tertiary, 203 -4, 204 511 Trypanites iclznofacies, 356, 358, 359 - 60, transport 359, 360 hydrodynamics tube-worm, feeding, 389 bones, 232 -5, 234 tubular fossils, 24 -5, 27, 29, 34, 443 plant material, 230 - 2, 2 3 1 , 351 , 352, TullinlOnstrum gregarium, 281 354 tunicate-like invertebrate, vertebrate shells, 226, 227-9, 228, 229

see also mammals

ancestor 114 tunicates coloniality, 330, 334 encrusters, 346 Tupaioidea, evolution, 440, 441 turbellarians parasites, 377 Precambrian, 30, 31 turbidity currents Lagerstatten, 240, 241 , 243, 286 Hunsriick Slate, 278 Turboella, 38 turnover rate, species, 185, 186, 186 turrids, predators, 389 Turritella, 228 turtles extinction, 202 evolutionary faunas, 39, 41 Lagerstatten, 292 Triassic, 194 type series, concept of, 524 type specimen, concept of, 524 Tyrannosaurus, 205, 207, 374 - 5 uintatheres, size, 150 Ulakhan-Sulugur, Aldan River, Siberia, 476, 477 ultraviolet radiation origin of life, 5 Palaeozoic, 60, 62 photography, 508 unconformities, geochronology, 483 Undina, 284 UNESCO, 522 ungulates, evolution, 86 - 7, 87, 137 uniramians, 65, 68 unitary organisms, coloniality, 333 United Nations Educational, Scientific and Cultural Organization (UNESCO), 469 univalved, skeletal type, 225, 226 Upper Hartfell Shale, Dob's Linn, Scotland, 479, 480 Upper Mississippi Valley, U . S . A . , 396 uraninite, Precambrian, 13 ureotelic nitrogenous excretion, terrestrialization, 69 urodeles, terrestrialization, 69 Urohelmintlzoida, 359

Vaizitsinia, 21 Valdai Series, Podolia, Ukraine, 1 7 vampyromorphids, Lagerstatten, 284 Van Valen's Law, 1 1 9 - 20, 120 vanadyl petroporphyrin, geochernical fossil, 96, 97 Varangian glaciation, 17, 1 80 varanids, Tertiary, 205, 206 variability, populations, 156 Variscan Orogeny, 277 vascular plants see tracheophytes vegetarianism, hominids, 89, 367 velocity profile, benthic habitat, 43, 43 Vendia, 21 Vendian diversification, 44, 48, 49 - 50, 51 evolutionary faunas, 40 extinction, 1 7, 22 - 3, 33, 44, 1 79 - 80, 1 80 metazoans, 1 7 - 23, 1 9, 20, 29, 30, 3 1 - 3, 32, 44 problematic taxa, 444

583

Index Vendomia, 21 Vendomiidae, Precambrian 21 vendotaenian algae, Precambrian, 17, 1 80 Veneracea, biofacies, 400 'Venice System', salinity, 406 Venn diagram, 43 1 , 433 Venus, compared primitive earth, 8 verbeekinid fusulines, 487- 8 Vertebraria, 265 vertebrates biomechanics, 321 coevolution, 138 coprolites, 366 - 7, 366 developmental patterns, 309, 3 1 0 diagenesis, 257 diversity, 131, 132, 132, 133, 134 evolutionary tree, 428 extinctions, 161, 191, 192, 193, 196, 202 feeding, 362, 368, 370, 372 flattening, 239 flight, 75 -8, 77 genetic variability, 328, 328 grasslands, evidence of, 85- 7, 87 heterochrony, 1 14, 1 18 Lagerstatten, 29, 239, 267, 286 Grube Messel, 291, 292 - 3 Holzmaden, 283, 284 Hunsriick Slate, 277, 279 paedomorphosis, 1 1 1 size, 147 skeletons, 27, 28, 314, 317 speciation, 108 - 9 transport, 232-5, 234 vesicomyid bivalve, trophiC structure, 389 - 90 Vestrogothia spina ta, 275 vicariance biogeography, 448 - 5 1 , 45U, 451 , 454 - 5, 457 viscosity, hydrodynamics, 323 vision systems, computer analysis, 497 - 8 vitrinite reflectance, thermal maturity, 51 1 - 2, 512, 513, 513, 514, 515 viverids, predators, 375 vivianite, Lagerstatten, 291 Vladimissa, 21 vola tiles, decay process, 214 volcanicity biostratigraphy, 483 -4, 490 extinction process, 160, ]62, ]63-4, ] 66, 1 67, 1 68, 169, 170 events, 203 periodicity, 1 77, 178 Grube Messel, 290, 293 organic debris, 96 Volvox-like green algal colony, 50 Vombatidae, extinction, 208 'Voorhies Groups', transport, 233

Waeringoscorpio, 67 Walcott Quarry, British Columbia, 271 Wales, sea-level curves, 488 - 90, 489 walking, biomechanics, 320 Walther's Law, biofacies, 398 Wanakah Shale, Lake Erie, New York, 242 Warrawoona Group, Western Australia, 10, 12, 51 , 338 water supply, terrestrialization, 60, 64, 65 water transport bones, 233 plants, 231 - 2, 231 water column overturn, 220, 221 waves destructive process, 223, 226 encrusters, 350 fossil concentrations, 236, 237 reefs, 345 shells, hydrodynamics, 228, 229 weathering, soils, Palaeozoic, 57, 58, 59 webs, graptolites, 52 Wegener, A . , 547 weight hominids, 88, 89 leaves, 230, 231 Weischselia, 265 Welsh b asin geochronology, 483 Welsh borderland, Silurian, 395 Wenlock Series, Silurian, 463, 464 West Tethys, biogeography, 457 Western Interior Basin, North America, 465 wetland herbaceous communities, 83, 352, 353 whales feeding, 365, 370 size, 150 - 1 whelks, trophic structure, 390 White River Badlands, 375 White Sea, northern U . S . S . R . , 32, 33 Whitwell Chronozone, Welsh borderland, 463, 464 Widdringtonites, 283 Wild-Leitz system, photograph, 508 wildfires, extinction, ] 69, 203 -4 Wilsonia Shales, 395 wind tranport bones, 233 plants, 230 - 1 Winteraceae, Cretaceous, 8 1 within-locality organization, 438, 439 within-sample organization, 438 within-species evolution, 106 - 10, 1 09, 1 19, 124 Wolstonian cold period, 383 wombat, size, 150 wood

biomechanics, 318 climate indicators, 402 diagenesis, 254, 254 evidence, 79 hydrodynamics, 231 wooded communities, Tertiary, 83 woodlice, terrestrialization, 65 Woodward, J . , ( 1 665 - 1 728), 539, 542 woody plants, Cretaceous, 81 working groups, Precambrian - Cambrian boundary, 476 worms Lagerstatten, 282 modern, 48 Precambrian, 30, 33 symbiotic, 138 see also annelid worms; platyhelminthes; polychaete worms Wyoming, Eocene primates, 109

X-ray photography, 508 xenosaurids, Tertiary, 205 xeromorphic habitat, 351 xiphosurans, 279 Xiphosurida biomechanics, 319 Lagerstatten, 279 living fossil, 157, 157 see also horseshoe crabs; Limulus

YeIlowstone National Park, U . 5 . A . , 266, 352 Youngibe/us, 284 Yudomski event, Precambrian, 35

Zilmerdak 'Series', Urals, 31 zinc bromide, sample preparation, 504 zone fossils, 466 - 7, 466, 467 zoological nomenclature, 417- 18, 419 Zoophycos, 260 ichnofacies, 260, 356, 358 - 9, 359, 412, 412 zooplankton cholesterol, 217, 2 1 8 diversification, 50, 51 , 52 extinction, 185, 189 ZosterophyIlophytina, Devonian, 63 Zosteropltyllum, 6 1 , 62, 63 zuglodonts, predation, 370 Zumaya, Spain, 201, 202 zygomorphy, Cretaceous, 83 zygopleurid gastropods, Triassic, 189