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

DISTRIBUTORS

Marston Book Services Ltd PO Box 269 Abingdon, Oxon OX14 4YN

(Orders:

23 Ainslie Place, Edinburgh EH3 6AJ 350 Main Street, Maiden MA 02148 5018, USA

54 University Street, Cariton Victoria 3053, Australia Other Editorial Offices: Blackwell Wissenschafts-Verlag GmbH

Tel:

01235 465500

Fax: 01235 465555) USA Blackwell Science, Ine. Commerce Place 350 Main Street Maiden, MA 02148 5018

(Orders:

Tel:

800 759 6102 617 388 8250

Kurrurstendamm 57

Fax: 617 388 8255)

10707 Berlin, Germany Canada Blackwell Science KK

Copp Clark Professional

MG Kodenmacho Building

200 Adelaide Street West, 3rd Floor

7-10 Kodenmacho Nihombashi

Toronto, Ontario M5H 1W 7

Chuo-ku, Tokyo 104, Japan

(Orders:

Tel:

416 597-1616 800 815-9417

All rights reserved. No part of this publication may be reproduced, stored in a retrieval system, or transmitted, in any form or by any means, electronic, mechanical, photocopying, recording or otherwise, except as permitted by the UK Copyright, Designs and Patents Act 1988,

Fax: 416 597-1617) Australia Blackwell Science Pty Ltd

54 University Street Cariton, Victoria 3053

(Orders:

copyright owner. First published 1990 Paperback reissue with corrections 1992 Reprinted with further corrections 1993, 1995, 1997

Tel:

3 9347 0300

Fax: 3 9347 5001)

without the prior permission of the

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

.!::!

�

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

Vl Vl «

�

� f-«

u.J

�

13:I

Vl 0 .D

'"


'" Vi 0

· Sed i m e n t­ water i n terface f-Z

�

0

u.J

V; u.J

3:

I Vl

:: .2


�

0

�

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-

<J.l <J.l ..c u - '" Q) 't: > <J.l 0 .D .S '" � - <J.l ..c-

�3 <J.l E I

<J.l

Ic

"0 <J.l <J'

Relat ive c u rre n t ve l o c i ty

T

B e n t h i c hyd rodyna m i c b o u n d a ry layer

Sed i m e n t­ water i n terface Fig. 2 Velocity profile of the benthic hydrodynamic boundary layer.

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;

E- E :7:Q;

-0 u Q; u ..c '" �'t:

E�

g .� Q; u c

�

0

Pa l aeozo i c

100 50 0

M esozo i c

....... .. . .- . . . . 1---- .-- .... •

•

•

..

•

• •

u

'0 N 0

c Q;

• •

U

-50

-100

100 50 0

-50

-100

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:

0

to

E � Cl! U

� .c:: c

2:: co 3: .'.

0 51 20J 10 •

Alcyonarians Sponges

•

Alcyonarians

A r c h aeocyat h i ds

_

C o ra l s

G ra ptol i t e s

c Cl!

E

B ryozoans

:;;

S ponges

u

5

Cl! > 0 ..0 co Cl! u c

�

0

•

A l cyona rians

A r c h a e ocyat h i d s G rapto l i t es

Co ra l s B ryozoans

0

Fig. 4

S ponges

1£ 10 ISI D Ic,IC21 P �rl J I K IPgIN� Q P a l ae ozo i c

Mesozoic Cenozo i c

Tiering history o f Phanerozoic colonial suspension

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

C r i n o i d ea

•••

�.:::::.::;: ....... _ •


:r


E

c

Parac r i n o i d e a I" :.,.. ..;.:. . ... , ::. ;. � :. .:-:.;, ..... : .' ., .. .... :.,. : ::..'."'. ::.,

if>

5

Para b l as t o i d e a

Ho l ot h u ro i d e a

R h o m b i f e ra

D i p l opo r i ta

•

v
o .D '"
B lastoidea

��� � � � � � � � � � � !! !!!! !! .:�

-;;;

Cri noidea

. Cri noidea

E d r i o a s t e ro i d e a

!!

Eoc r i n o i dea

••••••• B l a s t o i d e a _ Coronoidea _ Parac r i n o i d ea I: .. ::......... ,.!:: •••• R h o m b i fe r a

CS

�

�;:;;;;;;::����������

? I · ..., ..... ,., ..... , •..•. • "., ? ?

�

D i P I o po ri t a

I;;":'�-:'",;::,;:·:,::·.':.I Styl oph o r a S Homoste l e a I;,·.·.'.· :,i.�"... ·.: :'

,.a..:.,.\.. .:::�� Aste r o i d e a

.•

....... C r i n o i d e a

Cyc locysto i d ea

'

. . ....... . ... .

:

. '.1

Oph i u ro i d ea , .... ,: '. ::1

: : ::

E d r i o a st e r o i d e a ? I :···.· :.". ' ·:::· ·::····. ··:·: 1 Hom o i oste lea � He l i coplacoidea ••••• Eoc r i n o i d e a

� !!!!!�!!!!!!!�� •

I

o

E

::::I::-I 0 I si I I

• S u spe n s i o n

.::J·,;.·. ·.· : ..:: .::

D

Pa l aeoz o i c

KEY

rn S u spe n s i o n p ro m i n e n t

Cl

feed i n g

feed i n g habit q u estioned

C2

. ::

.

:. ; ;:.'. '.; ::... :':�.',:: ...

P

I

Tr

J

I I

K

Mesozoic

I

[2] S u spe n s i o n

U3 E c h i n o i d e a

. .. ..., :·1

I l

Pg Ng Q C e n oz o i c

feed i n g n o t pro m i n e n t

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

20

5

E � � u

-t

�

i

-

Hippu r i t o i d a Myt i l o i d a Myt i l o i d a Arcoida Hippu r i t o i d a

O ��------­

Pte r i o i d a

• F o rd i l l o i d a

_______ Praecard i o i d a ______ Act i n o d o n t o i d a

c

______ A rco i d a

______ Pte r i o i d a

______ Ve n e ro i d a ____ P h o l a d o myo i d a ______ Myt i l o i d a

-::::::::::

3:

o �

�

-

6 � � �

t(

o

______ Myo i d a _ Un ionoida

.D

�

S o l e m yoida

Trigonoida

- 6 ��-----

I

Pholado myo i d a Ve n e ro i d a Myti l o i d a Myo i d a

-1 2 .--�� T r i go n i o i d a

,J

_______ Pholadomyoida _____ Myo i d a

Ve n e r o i d a

Pa laeozo i c

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 .

u

o N

o c.:: L.LJ

Z « I 0...

5

0

"0 c
>

0

0 c.:: 0...

I

E d i ac a r i a n

I I

----

Va l d a i a n

V a r a n g e rlan

c '"
Ap h e b i a n

I

early

650

700

late middle

560

1

l a rv a l zoo p l a n k t o n agnostids c h i t i nozoans

1

a c r i t a r c h m a s s ext i n c t i o n (70% l o s s of t a x a )

pyrrop hytes

offs h o re h i g h d i v e r s i ty

?

zoobenthos

�

med u s o i d s

r o l e geo t h e r m a l v e n t s �

...

?

be n t hos

�

'I 1

3700

3500

t

Ediacarian benthos

t

Z O O P LA N KT O N

P R O T I STS

P H YT O P LA N KT O N a c r i t a r c h d i v e r s i ty p e a k

g r a p to l i t e b e n t h o s

,

o r i g i n of c o e l o m a t e z oo b e n t h o s

• I I

Ediacarian

....... '-J

H e c t o r G ro u p

I

B i t t e r Spri ngs Beck S p r i n g D o l o m i te Belt Su pergroup

Lower Belcher G ro u p G u n f l i n t C h e rt

2500

c.::

«

rad i o l a r i a n s a c r i t a r c h r e p l ace m e n t f l o ra

1 600

3 1 003200

« I U

p r ov i n c i a l z oo p l a n k t o n p re d a t o r y z o o n e c t o n g r a p to l i t e p l a n k t o n p ro v i n c e s fi rst M A C R O Z O O P L A N KT O N

1 400

Z « L.LJ

g r e e n a l ga e t o l a n d ( fo l l owed by f i s h )

1 000

l

w i d e s p read Lower P a l aeozo i c geosync l i n e & ocea n i c deposits & s h e l f sea deposits

c o s m o po l i t a n z oo p l a n k to n p re d a t o r y z o o n e c t o n

500

-€

N

c.:: L.LJ f-

438

o

c '"

U

Ma

B u l awayan Group F i g Tree Onve rwac h t

s t ro m a t o l i t e s i n shore shelf

? fi rst p l a n k to n i c bacte r i a

A N O X I U M I S O LAT E S

+

A N O X I U M c h e m a u to t r o ' P LA N T S '

tJ � . '"

....

Si
::::.

....

o· ;:::

� $: ::::. .... ;::i . '"

::r ....

�

::::. .... Vl

(Wa r rawoona l i g h t e n e rgy

G ro u p ) o u tgass i n g geot h e r m a l v e n t s

( lsua)

A N I MA L S

Fig. 1 Time and place in the origin and broad evolution of plankton. Inshore, shelf and slope environments are indicated diagrammatically to the left and right of the main part of the figure; narrowing oceans are suggested from the Cambrian to the Silurian; main depositories of the plankton record are shown in the right hand column and approximate time correlations to the left of the figure . The position of the Warrawoona and Isua rocks are shown in parentheses .

CJ1 >-'

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) .

400

D

�

0

0 5 N

0

z « u.J

600

1f t V

1000

I I I I I

<> I v �

.c

ro

� <JY � '" o N o

c

C

co

>­ u o Q) '" .c u

800

The Precambrian Reefs extend well back into the Precambrian (Copper 1974; Hecke1 1974; James 1983) . The earliest unquestioned stromatolites (see also Section 1 . 2) are from the Fig Tree Group of the Barberton Mountain Land, South Africa, 3300 - 3500 Ma . They are regarded as the product of a photoresponsive microbial community in a shallow, evaporitic environment, and associated microfossils include filamentous forms . There is no certainty that the microbes are true cyanobacteria but already a range of stromatolitic forms from linked domes to pseudo columns is present . The stromatolitic car­ bonate ecosystem became widespread some 2500 2300 Ma (Fig. 1 ) . Our knowledge of the evolution of the microbial communities responsible is vague but increasing . Most were probably eubacteria, but true cyanobacteria may not be very old . Eighteen mor­ photypes are known from the 1600 - 2000 Ma Gunflint Chert in Canada; most are of blue-green appearance but many are of unknown affinity. In Australia, the 1600 Ma Paradise Creek microbiota is morphologically comparable, and the 800 - 1000 Ma Bitter Springs community is extremely similar to that of modern stromatolite communities (Walter 1 976) . Early Proterozoic stromatolites ranged from non­ marine to deeper-water environments . Extensive shelf biostromes, mainly of linked domes, grade into shelf-break bioherms with several metres relief of branching columnar morphs in the Slave Province of Canada . Individual build-ups reach 100 m di­ ameter and 20 m thickness . They are cut by channels draining the shelf and die out rapidly down slope into the basin . Although extremely simple ecosys­ tems, these are regarded as positionally and func­ tionally comparable to modern reef ecosystems. Elsewhere stromatolitic masses on Proterozoic shelves < 60 m thick and 1 - 2 km long are reported. Precambrian stromatolites tend to be larger than

U

u N

0

Z «

.:;:

I Cl... u.J

�

�

0 Iu.J

Ma

� Cl...

0

2000

3000

I U � «

C u m u l a t i v e t h i c kness I

m

!

Fig. 1 Distribution in time of the major reef building biotas of the Precambrian and Early Phanerozoic.

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

60��____�____�______+-____�____��____�60

o r-------+---��+_��-,����--�-+_� O

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

58 Cz U

0 N

0 u.J :2

V1

<5 <J>

<J>

�

<J>

� .D 2 .!::! :2

�

�::J

<J>

U >£ 0.. 0 C

u <J>

? -0 '"

'l)

CCl

'6 0 �

C!2

.�

o

E 'l) -0 0

::J 0 00 '" £ 0.. 0 u <J>

E

'"

� 0.. -0 'l) $

g

::J .D c le

'0.0 £ V> -<

E

>-

�.

C!2 0 <J> 0 'l)

0 00 C ..2 'l) a; u

cle £ u � 'l) <J> 0 0..

0 u <J> le $ ..2 -0 ::J

0 u 'l) :s � 'l) -0 'l) 2

E

>-

E

"0 'l) ::J C 0 � <J>

-'

E

t: <J>

.8 � .!::! c 'l) -0

� ..s

.� .D �

C le C

::J £ c le

�.

�

;.;:

<J>

E

::J

<J>

<J>

"l!

u...

:>

�

<J>

...L 1 900 M a Abiotic soils

Fig. 1 Geological ranges of major soil categories and first known appearances of important soil ecosystem components .

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

STRAT l G RA P H Y

2

Emsian

et

a;

o > UJ Cl

Cl

Z

c Q) OD

,,!!

'"

c

�

c

'50

,�

z

o

3:

Q)


c '"

...J

,�

c

'S:

o

"

...J

I

Pi'id o l f

0/

c

,!::

"0 Q)

r

LJ

I

Ludford ian L u d low Gorstian

z « Q;1

::> ...J
_

H o m e rian

S h e i nwood ian

Uandovery

I

tCI:J

Rhuddanian

Cl: S:!

0>

Ashgi l i

Caradoc

I

4J 1

rf\ \J0

Aero n i a n

------1 g � L--

(J)

0-

We n l oc k

Telyc h i a n

I Z

'

�

o -'" ..c u o

I

H I G H E R PLANT M EGAFO S S I LS

CUTICLES

I I

,

� ---"

\

I

,,

'r

,

I -' ,

I ,

1

N E MATO P H YTA L E S

l

ALGAE

1

FUNGI

5 6 7 8 9 1 0 1 f '1 � { 1 5 1 6 1 7 1 8 1 9

4

3

,�

c '"

c

I

S PO R O M O R P H S

,. >w. -Uil

1

� v

VI I 11 1

'

I

I

" . I 61

I

I

f-.-I

00

� ....,

�...... ....,

N'

� ...... ::::.

c' ;::

1

Fig. 1

g 1

F i rst appearances and strat i graph ic ranges of m i c ro- a n d m e gafoss i l s relat i n g t o colon izat i o n o f l a n d b y p l a n t s , R , Z a n d T refe r t o i n i t i a l m a j o r rad i a t i o n s of t h e vasc u l a r p l a n t s u bd iv i s i o n s Rhyn i o p hyt i n a , Zoste ro p h y l i o p hyt i n , and T r i m e rophyt i n a respective l y , F o r m o re co m p l ete explanation of see text.

1 -1 9 ,

0\ .....

62

1 Major Events in the History of Life

obscure, as vascular tissue has never been demon­

from sterile axes occur in the northern hemisphere

strated .

Ludlow . The earliest

direct

evidence for stomata

(with two guard cells) comes from sterile axes at the

4, 5. Monads with triradiate marks.

The earliest

base of the PHdoli, with examples on

Cooksonia and

monads not derived from obligate tetrads are

Zosterophyllum

smooth walled, usually with equatorial thickening,

ever, since stomata were described on Canadian

e.g.

Ambitisporites Cooksonia pertoni

recorded in the Gedinnian . How­

which is later recorded in PHdoli

Emsian

sporangia.

ably also present on the earlier Australian Ludlow

Sculptured monads

occur continuously from the Homerian, showing

they were prob­

Baragwanathia abitibiense

B. longifolia,

where cells are not preserved.

rapid diversification and increases in numbers in the Ludlow and PHdoli. For the most part their origins, be they bryophyte or tracheophyte, are unknown,

but

their

presence

Gedinnian

Cooksonia pertoni

in

Silurian

(Fanning

et al.

and 1988)

indicates that some of the producers may have been rhyniophytoid

(10) .

Higher plant megafossils

9. Sterile axes.

It is usually accepted that those with

dichotomous branching and peripheral support tissues (sterome), the earliest being Llandovery

Eohostimella,

are derived from erect land plants .

Late Silurian and early Devonian examples (e . g .

Cutic1es

6. 'Nematothallus'.

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 .

V) u.J l-

< I

u.J

STRAT I G RA P H Y

0

U

0 z N

U

Q u a t e r n a ry Neogene

0 �

U

\

0 ....J

I

0 I CL 0 I U V) >- z z< 0 0<'

V) 0

0 CL :::; 0<' >�

I

I

V) 0 -

0<'

:J u.J

U V)

:::

V) IU

CL >0<'

V) Z u.J

z 0 0: 0<' 0

V)

V) 0 -

z O<' I u.J U I< 1- 0<' 0<

I I I

Palaeogene

0

0 N

!

J u ra s s i c

I I I I I

Triassic

I

I

r I

I

0

U

0 u.J < ....J < CL N

Devo n i a n

I I

S i l u ri a n

I

I

I

I I

I I I

I

I

I

I

I

I } �

I

I

7J I I I

I

I Cambrian

Fig. 1

I I

I I

I

W

I

I

I I

I

I

I I

I I

I

f : t::

/

I

I I I I I I I

The fossil record of terrestrial invertebrates and

I

I I

Z

CL

:J ....J

I I

I

I

I

�

I

I I

I

I

�

I

I

I

I

I

I

I

I I

I

I I I

I

I I

I I

I

Key

Terres t r i a l record

1 I

A q u a t i c record

I

I

I I

I

their forebears.

<

0 I

I

I

0 �

I-

-.

I

I

a:l

u.J

0 0<' CL

I

I

I

V)

V)

U

I

I I I

U

0

< 0<'

V) -

�

I

I

z < 0<'

V) a:l

I I I

I

I

0 CL 0

--

I

" \ \ '\ i l ! !, ' i' , ! j )

I I

I

I I I

O rd o v i c i a n

I

�

I

Pe r m i a n

C a r b o n i fe r o u s

if

\

U

V) 0

I

�

C re t a c e o u s

I

V)

I

I I I

I

�

0 CL I CL � <

I

u.J

V) u.J

V) 0

I

I

I

I

I

I

I

I I

� 1

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 .

76

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

88

Ma

0.1

� ��I �{

1 .0

-

2.0

3.0

Homo sapiens sapiens

I --------f'

1)�O �

------

g�

Tool behaViou r -_

TERRESTRIAL

I

Homo sapiens neandertalensls 0 .5

89

1 . 1 2 Hominids

--J

Homo habilis

);,, -

:/.7;: ".

""tu,

��:

r;Z;;;� ' ...\' ��, ---1 f.t'

-

1

�df

d .,

b

Australopithecus a frican . .

�

------- 1-------1

4 . 0 ----i

5.0

-------����--

ARBOREAL

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

98

O rga n i c c o m p o s i t i o n of fo s s i l sca l l op s 500 ,----,- 30

ti1 Qj

-G- A m i n o acids

Q.. 00

�

300

'u

'" 0 c

200

C

-+- % s u rv i v i n g

400

20

'" >

.�

<Jl

«

E

er:

�

"0

'E

QJ u (lJ

::l

10 C

<Jl

�

(lJ

(lJ Cl..

1 00

Pleist

Plio

Mio

lur

e ret

Olig

G e o l ogical period Fig. 2 The progressive decay of organic compounds from the shells of fossil scallops with time . Approximate ages, in millions of years, for the horizontal axes are Pleistocene (2), Pliocene (4), Miocene (15), Oligocene (30), Cretaceous (100), and Jurassic ( 1 75).

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

O rga n i c c o m p o s i t i o n of fos s i l sca l l ops 500 -r--------------��------------------�------------__,

IS] IiJ;!I •

I n s o l u b l es S o l u b l e peptide Free a m i n o acid

e ret Geologica l period

Jur

Fig. 3 Proportions o f free amino acids, soluble peptide fragments, and insoluble organic residues in the shells of scallops of various ages. Horizontal axis as in Fig . 2.

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

100

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

D i p l o i d hyb r i d

U n b a l a n ced gametes

Tetra p l o i d h y b r i d

X

I

Pa rent 2 A'A' B ' B ' C ' C '

{[ AA' BB' CC'

I

AA ' CC

BB

AA A ' A ' B B B ' B ' C C C ' C '

D i p l o i d gametes Fig. 1 The effect of polyploidy in restoring normal segregation in the Fl hybrid between two diploid species with three pairs of chromosomes. Note that a cross between the tetraploid hybrid (which produces diploid gametes) and either parental species will result in a triploid offspring. Such an individual will have low fertility, owing to the production of unbalanced gametes in meiosis .

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

104

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-

106

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

G

II

s �:� S S

LQ PH

EP

Q�

/1

Nilelds

C n e m i d opyge

Berga m l a

43

19

"

:�

WL

"

B G ---,-",--� ---, ---r". 2

3

6'0

---,--,---.---�---,--, , '-"' , I ---,--.-,---� --, ---,---r-' 6 5

r ,

�

P l atycalymene '3fH ) .

"

109

Ogygioca re l l a

.

)' �' t {

W h i ttard o l i t h u s

Ogyg m u s

"

8

-4, r--"T�--,--",

r--"T�---,--,---, '

N u m ber of r i b s

"\"

� 9

11

T

5

12

/ /.

11

�1 { x1

525

'

N o b i l iasap h u s

13

---,-� - ' , 1 ---,-,--;-4

"--,r,-r-�--,--,---, , "", 9 10 11 1 2 1 3 14 1 5 1 6

Fig. 1 Summary of changes in mean number of pygidial ribs for eight Ordovician trilobite lineages in the Builth inlier, central Wales. Means with 95% confidence interval and number of measurements are shown by -n and : n. Approximate mean ( 0 ) . Data from Hughes (see Sheldon 1987) (H) . Individual measurements (Xn) . Successive means (1) are significantly different at the 95% confidence level. Successive means (rJi> are certain to be significantly different but full data are unavailable. Vertical spacing between sections (BC, etc. see Sheldon 1987) is not to scale . Reversible shifts in means are common within sections (not shown subdivided) . Sections in the Teretiusculus Shales span c. 3 million years. (From Sheldon 1987.)

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

112

Pr o g e n e s i s c

1

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 .

1

Post-d i s p l acement A

B

00 8

c

Neoteny is reduction in rate of morphological devel­

1

N eo t e ny

A

B

c

o H

Post-displacement occurs by changes to the timing of

11

A n cestor B

08

C

G

opment during juvenile growth . If maturity occurs at the same age in both ancestor and descendant, they will be the same size . Often onset of sexual maturity is delayed in neotenic forms, consequently the neotenic forms attain a larger adult size. Neoteny may be global in its effects on the organism, or dissociated when it affects only certain morphologi­ cal structures . Reduction in degree of allometry of specific structural elements will result in neoteny. Unlike progenesis, where the juvenile ontogenetic trajectories of ancestor and descendant are alike, juvenile growth trajectories are different between ancestors and descendants .

D

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 .

2 . 4 Heterochrony

1

Hype rmorphos i s B

c

E

D

Prp.ri i , n l .::ll rpmpnt D

A"C' D

Acceleration of rate of morphological development during ontogeny will produce a peramorphic descendant . In allometric terms, acceleration is an increase in the degree of allometry . For meristic characters it is an increase in the rate of production of structures . If acceleration is operating only on specific structures, then there need be no overall increase in body size . However, the particular struc­ ture is likely to be larger . As with neoteny, juvenile ontogenetic growth trajectories will be different in the ancestor and descendant.

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 .

E

Acce l e rat i o n

c

1 13

''11

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) . =

=

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 . )

114

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

116

Ontogeny

== ==> = :::== ========= c:::==

Periporal a rea

R EC ENT -T'"" l E!>! I S=� C:'= P-:-: O'-> E N E --I

B

?��

• • •

"C,

d

T.

PI�iio;m P.

doederleini

australis

PLlOCENE

MIOCENE

U

Z

w

. .

..

.

o S:2

--... ...P.antia us tralis

o

. . . . _--_. P. philipi

T.

coela ta

T.

U 8

OLlCOCENE

Z

squamosa

w

P.

prea ustralis

U 8 ;f: Z

w

E O.C E N E

...J

Se d i m e n t g ra i n size

", '

•

,, ' •

. .. Q •

•

• <>

= :> == = === :::== c:::=== E n v i ro n== m e ntal ==== grad i e== nt

Fig. 4 Peramorphocline in the evolution of the periporal area in the Cenozoic spatangoid echinoid Protenaster. Later species underwent greater morphological change in this character than earlier species. This led to the ability of later species to feed from progressively finer grained sediments . (From McNamara 1985 . )

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

T.

�

= > =====::::=== =� > ::::=.::=::

O NTOG E N Y

boongeroodaensis ( j u ve n i l e )

T.

/"�'"

.�

boongeroodaensis ( ad u l t )

Fig. 5

Paedomorphocline in the evolution of the umbonal region of the Cenozoic rhynchonellid brachiopods Tegulorhynchia and Notosaria, showing paedomorphic retention of larger foramen (and hence thicker pedicle) and smaller umbonal angle. The environmental gradient along which the paedomorphocline evolved was from deep to shallow water. (From McNamara 1983 . )

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 .

2 . 4 Heterochrony Proge n e s i s/ acce l e rat i o n

OIl

r OIl

LOW

..

•

S e l ectio n

•

N eot eny/ hype r m o r p h o s i s

Stab i l ity

•

HIGH

H eteroch rony

O rgan i s m s i z e

•

k

LARG E

Water depth

Fig. 6

Diagrammatic summary of McKinney's (1986) proposed relationship between water depth, ecological stability, selection, organism size and heterochronic process, based on a suite of Tertiary echinoids from southeastern U.S.A.

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

A

•

( ,,)

1 000 -

•

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) .

.

"""

•

Ext i n ct

" Living

1 00 -

•

•

. .

"' '''

••

-

1 0 --= -

-

'"

•

•• ...

.._.

I

I 200

I

o

(1 06 y r s ) B •••••

1 000 c:

•

•

•

••

••

1 00 -:

• •

•

•

•

•

•

•

", ,,, ,,, ,,, ,,,

1 0 -: •

.. ••• " "'.

E xt i n ct

'" L i v i n g

o

•

I

10

••••

T 30

Fig. 1 Taxonomic survivorship curves for A, pelecypod (bivalve) and B, mammalian genera (major Therian orders). These graphs show roughly linear trends, and indicate constant probabilities of extinction for genera of any duration . (After Van Valen 1973 . )

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

122

C o n stant e n v i r o n m e n t B

A 1 00 bO C

;;:

.� .

:::J '" '" Q)

'u

Q)

1 00 ,-----Stat i o n a ry model

Red Q u ee n model 10

10

a. Vl

B

A 5

5

10

10

Species d u rat i o n

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

Pe r i o d i c a l l y d i st u rbed e n v i r o n m e n t

C

D

1 00 bO C

;;:

.� .

:::J

'" Q)

'u

'"

1 00 bO C

;;:

.�

Red Q u e e n model

.

:::J '" '" Q)

10

'u

Stat i o n a ry model 10

Q) a. Vl

Q)

a. Vl

C

Fig. 2

D 5

10

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

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

00 c

.�

.:;

:J

A

'" 2 . 1 6 '� ,,0 "f", 1 .92 ".b", "k , 00 , ,, 1 . 68 " 2 .40

"

'u Q) Of>

Q) 0..

00

Of>

-'0

C

1 . 92 1 . 68

1 . 68

1 . 44

1 .44

I

'..,cm "l'"" "'-,()

1 . 20

'?ro '0

1 . 20

0 0

'" 2 . 1 6 ,,.00 ,� ,0000 1 . 92

2 .40

2.16

0 <xl

1 . 44

Of>

B

2 . 40

.96 . 72

_ 0 ,11""" aDID

.96

-

.24

,

0 '-:----:.':---'"--="'---"'--=0::-- ' '& 50 40 30 0 20 0 10

.48 .24

1 . 20

..,

. 96

o

. 72

IIIGllDI

.48

,

. 72

0

.48

=

o

10

20

30

40

50

.24 60

°0

,, 00 ,. ,

,i'

,a.o """0 0 ,

, a>

'';?

0 10

,d 30

I 40

I 50

I 60

Du rat i o n (1 06 yrs) Fig. 3 Species survivorship curves for A, coccoliths; B, radiolarians; and C, planktic foraminifera. Each graph contains data for three cohorts - taxa arising in the earliest Pliocene, in the latest Pliocene, and in the Holocene, and each is represented by a different symbol. (After Hoffman & Kitchell 1984 . )

Tempe rate

Tra n s i t i o n a l 0.5

0 P l e i stoce ne 2.0 4.0

Pl iocene

-''"

8.0 10.0

>'f::, 1 2 . 0 s Q)

.§ I-

1 4 .0

Q) C Q) U 0

'i

�

"0 "0

'i

20.0

N 21

N 16 N 15

N 14 N 12 N ll

N 10 N9

16.0 18.0

N 22

.'l:!

6.0

-;;;

0 . 1 0 .2 0 .3 0.4 0.5 0 .6

NB

�

>-

u.J

N7

N6 N5

22 . 0 24 . 0

Latest O l i gocene

Fig. 4 Extinction rates for species of Neogene foraminifera for the whole of the oceans ('total'), and for tropical, transitional, and temperate assemblages, for the past 25 million years (latest Oligocene to Recent) . The 'N' zones are standard Neogene planktic foraminiferal zones. Peaks in extinction are correlated globally, and linked to major changes in the physical environment. (After Wei & Kennett 1983 . )

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

A O rders

B

800 Fam i l i es

c

1 00 Genera

50

1 00

D

50

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 . )

132

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

I' .., r , I I I j I , 1 1 , 1 1 1 , 1 1 1 , 1 I I , t 1 1 , 1 J I I I 1 1 1 1 1 ' I ' 1 I I 1 , 1

A

10

600

Vasc u l a r p l a n t s p e c i e s

B

300

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

A

. . .. . . · . ... .. . · . . . . . . . . · · . . . . . . . . · · . . . . . · . . ·

::::: :: :::::::: . . . .. ::: :::: ::: :: :: : ::::: :::::: :::::::: . . .. .

. .. ... . .. . . . . .. . . . . .. .. .. . .. .. .... . .. .. . . . . . .. ..

. . . .

.

::::: ::: ::: :::: : : :: :::: : . . .

. . .. . . .

Speci es/Myr

. . · . . . · . . . · . . . · . . . · . . . · . . . · . . . · . . .

· ·

· ·

. .

. .

. .

· . . · .

.

A l p h a d i versity

·

.

.

.

. . . .

· . · . · . · . · . · . · . · . · . · . · . · . · . · .

. . . . . . . .

r"T"l......,,..-I;I��� I ��I� m�t D

G e n e r i c d i ve r s i ty

E

F a m i l ies

.

.

.

.

.

���t�

:..:..:..:..

. .. .. .. . .. .. .. .. . . . . . . . . . . . .. . . . .

. .

.. .. · . . . · . . . · . . . . · . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . .

. .. . .. .. .. .. . ... .. .. . . .. . .. .

· . . · . .

.. .. .. · . . . · . . . · . . . · . . . · . . . · . . . · . . . · . . . · . . . · . . . · . . . · . . . · . . . · . . . · . . . · . . . · . . . · . . . · . . . · . . . · . . . · . . . · . . .

· . . · . . · . . · . . · . . · . .

:::: :: ::

.. . . ...... ... .. . .. .. . . . . . . . .... .. .... .. . .... .. . . .. . . .. . .: . : . : . : . ·

o

·

· . . · . .

·

. .. .. . . . . . .. �;-o"Im;... .... .. . : . : . : . . . . .. . . . . . .

.

ff

·

·

C

· . . . . · . . · . . · . . · . .

·

·

B

. .. .. .. . ·. . .. . .. . . . . .. . .. . .. . . . ... . . .... .. .. ... .... .

Trace fos s i l s

. .. ... . .. . .. . . .: . .

......... . .. .. . . ... .. . .. . . . . . . :. : . : .

. . . . .... .. ... ... . . . . .. .. .. . .. . . . . .. . . . .. . . : .: . . . .

...... ... . . . .. . . .. . . . . . . .. . . . .:

:

. .. . . . . . .. . . . . : .:

5

D

C

P

Tr

. . . .. . . . .. . . . . .: . . . . . . : .: . :

. ·.. ...... .. . .. . . . . . . . . .. . . . . . . .. .. . . . . .. . . . . . . . .. . . : . .. .. . K

.

.

.

· . . . · . . · . . · . .

Ce n

Fig. 3 Trends in marine animal diversity through time . (After Sepkoski et al. 1981 . ) The five trends in diversity accepted as evidence against an equilibrium model of Phanerozoic diversity. A, number of the trace fossil genera within individual habitats . B, numbers of described species, normalized for length of the geological period. C, alpha diversity of marine invertebrates . D, E, numbers of genera and families respectively . The original figure was presented without vertical axes, as shown here .

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-

137

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,

138

2 The Evolutionary Process and the Fossil Record

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,

139

140

2 The Evolutionary Process and the Fossil Record

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

141

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

142

2 The Evolutionary Process and the Fossil Record

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

143

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

144

2 The Evolutionary Process and the Fossil Record

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

156

B

A 4.5

v; c:

.�'"

� V

�

>-

;;; c:

.g::J

(3 >

L.U

4.0

3.5 3.0

1 2.0

f, ,, ,

1 .5

1 .0

c:

V

�

C '" c: o

.�

EXT R E M E C HAN G E

(3

, 1 1 ,'", " , ,

40 . 20

-'

o

I

0

'

I

EXTRE M E C H A N G E

o ,

04 o o

�'

, , " 1 1 33 2 ' " " , , I

·4.0

I I

'------'-

· 2 .0

�, , ,

o , o

6 .0

c:

,

0

o o

8.0

L.U

2 I I l 2 2 3 15 2 2 ' 2 1 5 2 5 5 5 2 '2 I [ 5 :5 4 X 6 X I X '2

�

1 0.

>

,

21 1 12 I 423 2 1 4 1 3:':5 4XXS 23XX'X o 42XX9

0.5

�

�

0

"' �

.� ,

2. 5

2.0

v;

J

o

4 16

I

� I II : 1 2 1 1 4 1

2'0

I

30

t

'2

40

Meas u re m e n t i n te rval ( 1 0 6 yrs)

5'0

.6

.0

NO MEAS U RA B L E C H A N G E

" f

, , , 1I I

I

I I

I 13 :5 '2 I 1 1 21 1 2 2 212 2 1 '2 33551 2 1 1 '2 23�(' I 1 1 85 I I I 1 21 534 19 2 2 34 1 33 2 I " !�i ' '2

I 1 1 24 2 t 1215 31 I 31 2 41 1 1 1 1 3 3 . 33 I 2 2 1 32 1 1 I 3 1 1 1 32 4 1 2 � 1�4 �J k3 1 ' I t 1 86 I 412 1

'"

4.'"'" 6 r---:c --= . 2'"'"" 6.-=. 8'"'"" .o --' . 6'"'"" � .o --c " . 0 --=' rc .'O .0-"""' .1 � .0 -.-' 0 4c:.0 -02c:2 . 0-1 4.o--

Ln Meas u re m e n t i n te rval ( 1 0 6 y r s )

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

A

� Morpho l ogy

B

C Fig . 3

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

-

2 . 1 2 Mass Extinction: Processes -¥

-¥

P l i oc e n e- P l e i stoce n e M i oc e n e

S e a l evel

\"

..J

O l i gocene

Pa l aeoce n e & Eocene

�*

� \� *

Cretaceo u s

J u ra s s i c

Triassic

Pe r m i a n

Carbon ifero u s

Devo n i a n

S i l u rian

O rd o v i c i a n

Cambrian

�

(* \

"\

* --

(*

\*

�

Fig. 1 Phanerozoic sea-level curve with Newell's (1967) six extinction events shown as asterisks . High sea-level to left. (After Hallam 1984 . )

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

162

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.

163

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-

164

2 The Evolutionary Process and the Fossil Record

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

165

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

166

2 The Evolutionary Process and the Fossil Record

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-

167

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

170

2 The Evolutionary Process and the Fossil Record

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

172 Pe r i od i c :

I

R a n do m :

11

I I I I

II

I II

I

I

I

I

I I

Fig. 1 The contrast between a periodic and a random time series . Both series have the same frequency of 'events', but the random series is characterized by irregular clusters of events with variable gaps between them. (After Sepkoski 1986 . )

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

173

70 50

30 20 c

.Q U c

xQ) Q)

�

10

c

Q) 0-

S

1 00

1 50

200

250

50

Geological t i m e ( 1 0 6 yrs ) Fig. 2 Raup & Sepkoski' s (1984) time series for familial extinction from the Late Permian to Neogene, computed from their highly culled sample of marine animal families . The 12 'peaks' of extinction are highlighted by stippling, and the fit to the 26 million year periodicity is indicated by the vertical lines (note the lack of fit in the Middle Jurassic and Early Cretaceous) . Geological systems and stages (small boxes with initial letters of names) are indicated along the bottom of the graph (note the variable stage lengths, especially through the Cretaceous and Tertiary) . The y axis is logarithmic. Abbreviations along the time axis: D Dzhulfian; S Scythian, A Anisian, L Ladinian, C Carnian, N Norian, R Rhaetian; H Hettangian, S Sinemurian, P Pliensbachian, T Toarcian, B Bajocian + Aalenian, B Bathonian, C Callovian, o Oxfordian, K Kimmeridgian, T Tithonian; B Berriasian, V Valangian, H Hauterivian, B Barremian, A Aptian, A Albian, C Cenomanian, T Turonian + Coniacian, S Santonian, C Campanian, M Masstrichtian, PI Danian, P2 Upper Palaeocene, El Lower Eocene, E2 Middle Eocene, E3 Upper Eocene, 0 1 Lower Oligocene, O2 Upper Oligocene, MI Lower Miocene, M2 Middle Miocene, M3 Upper Miocene, P Pliocene . =

=

=

=

=

=

=

=

=

=

=

=

=

=

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

=

=

=

=

=

=

=

=

=

=

=

=

=

=

=

=

=

=

=

=

=

=

=

=

=

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

174

40 r--r----�--r_--_r--��

26-Ma Periodicity

30

c

.9 U c

xQ)

C :::

Q)

Tith

Q) Cl..

Fig. 3 Percent extinction for all marine animal families based on a data set with 970 extinctions . Peaks that are 'significantly' higher than background are labelled . (Guad Guadalupian, uNori Upper Norian or Rhaetian, Plie Pliensbachian, Tith Tithonian, Ceno Cenomanian, Maas Maastrichtian, uEoc Upper Eocene, mMio Middle Miocene, other abbreviations as in Fig. 2) . Error bars indicate one estimated standard error on either side of the data points. The y axis is a square root scale. (After Sepkoski & Raup 1986, by permission of the AAAS . ) =

=

=

=

=

=

=

=

250

200

1 50

1 00

Geological t i m e (1 0 6 yrs)

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

50

o

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

175

2 . 1 2 Mass Extinction: Processes I

Guad

50

26-Ma Periodicity

Fig. 4

Percent extinction for marine genera. (After Sepkoski 1986 . ) The data illustrated comprise 9773 genera, of which 5594 are extinct. Note that peaks of extinction (labelled as in Fig. 3) are better defined than in the total familial data, and a seemingly periodic Aptian ( Apti') peak appears in the Early Cretaceous . No clearly periodic peak is present in the Middle ]urassic, although low, possibly spurious peaks appear over the Lower Bajocian and Oxfordian; a peak also appears over the Carnian within the Late Triassic. '

c o

"-6

40 Maas

uNori

c

xQJ 30

C QJ

::'

QJ 0...

20

250

(1986) did suggest a possible longer (greater than 30 million years) periodicity in the late Palaeozoic .

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

200

1 50

1 00

50

o

G e o l ogical t i m e ( 1 0 6 yrs)

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

176

2 The Evolutionary Process and the Fossil Record

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

B

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

c

2 mm

f------i

Three ichnogenera known from the late Vendian . A, Harlaniella. B, Neonoxites . C, Palaeopascichnus . All three are shallow deposit feeding or grazing, horizontal bedding plane trace fossils .

Fig. l

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 .

1 00

\ \ \ \ \ \ \ \ \ \ \ \

80 rti ;;.. ;; �

60

�

40

'"

c:

IJ) u

0..

�

20

O�

----- -

Trilobites. Only about 14 o f the 38 families o f Middle Ashgillian trilobites survived into the Silurian. The main decline in diversity occurred at the end of the Rawtheyan when about 15 families disappeared. Generic diversity which had been fairly constant throughout the Ashgill declined by 45- 75% at the top of the Rawtheyan (Fig . 1) and species diversity was possibly reduced even more .

/

/

/

/

Brach iopods ( 1 57 gene r a ) Trilobites ( 1 1 2 gene ra )

�____�____�____�____�____� c c c c c c '" Cl Cl Cl Cl Cl >>C C (j) GJ c Cl C .c Cl -0 � 0 -0 :: � :; Cl � 0.. Cl U I .c � �

__ __

The Late Ordovician extinctions involved signifi­ cant changes to a number of groups :

/

/

/ /

.�

Fig. 1 Percentage survival of genera from stage to stage in the Upper Ordovician, e . g . 98% of Cautleyan trilobite genera survived into the Rawtheyan and 25% of Rawtheyan genera survived into the Hirnantian. The graphs are based on genera found in sequences with good stratigraphical control mainly in Europe. (After Brenchley 1984, by permission of John Wiley & Sons Ltd . )

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).

183

2 . 13 Mass Extinction: Events z « et:: =:l

Vl

...l

Bathy m e t r i c cu rve Rhuddanian

� <...

�

{

)

::;

U

;; 0 0

H i rnantian

I ce caps m e l t C l i mate wa r m s D e e p flood i n g of s h e l ve s

4

G la c i a l m a x i m u m M ax i m u m regre s s i o n S h e l ves l a rg el y e m e rgent

, ( ...

Z

B i ot i c c h a n g e s

E n v i ro n m e n tal c h a n g e s

{

Low d iversity b i ota starts to d ivers i fy " , ,, ,,o,, ''' ' '' 0 ' 0 '' r W"OO",,', �,;,"nh» Ext i n ct i o n of s h a l low s h e l f b i ota ( brachiopods, corals, & ostracodes)

Pos s i b l e ext i n ct i o n o f s o m e s h e l f b i ota ( b rachiopods & corals)

.�

c

.s::: u

'"

E'"

et::

0

CJ �

{

Res i d u a l c o s m o p o l itan Hirnantia fau n a

G m�h of G o " d " " , ke coP' S p read of float i n g ice C l i mate coo l s Sea level starts to fal l Pos s i b l e ocea n i c ove rtu r n

�

i

M'f 0' ,," ,,0 ,,," of dcc P ; h" f "" " , h f , fa u n a s ( trilobites, cystoids) Maj o r ext i n c t i o n of graptolites Ex t i n c t i o n of conodonts & acritarchs in t h e t e m perate reg i o n s

Rawt h eyan

Fig. 2 Summary diagram showing the Late Ordovician- Early Silurian bathymetric curve and associated environmental and biotic changes .

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

Temperature. There is evidence from the wide

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 . =

=

=

=

=

=

=

=

=

1 0 6 yrs

=

U Vl Vl

::;

c:.: I-

=

=

'" c

D i e n e ri a n

:J "1:l c -

�

Cyronites Zone Ophiceras Zone Otoceras Zone

G r i e sbach i a n

M i xed Fa u n a 3 M ixed F a u n a 2 M i xed Fau n a 1

248 Changhsi ngian Dz u l fi a n 253

I--Z

� �

258

263

� UJ Cl...

'" .0.. c

Kazan i a n

� ?

:J

Qi "1:l '" <.J

:J

.� c

"1:l

�

c 0 Q) -J

I--

Palaeofusulina Zone N . C h i n a & S i be r i a c o l l i d e

Con t i n u ed c l i m a t i c osc i l l at i o n s

U fi m i a n

2 Permian and lowest Triassic geological stages, Permo-Triassic boundary biostratigraphic zones, and major tectonic and climatic events. Most workers consider the Palaeofusulina Zone the final zone of the Changhsingian Stage, and the mixed faunas the lower-most units of the Triassic . The Gyronites Zone marks the Greisbachian- Dienerian boundary. (Geological dates from Harland et al. 1982 . ) Fig_

Kungu rian

-

A rt i n s k i a n

268 Sakmarian

Asse l ia n 286

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 .

�

�

-r-

r-

E . E u ro p e , Kaza k h stan & S i be r i a acc reted

Pe r m o-Ca r b o n i f e ro u s g l a c i at i o n

189

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

30 g .� . 20 .§ Cl!

C x

10 500 .!!!

o

�

Cl!

Cl! a..

400

on

�

E 300

� o z

200

A

S

L

G

O

D

A

L

C

N

R

Triassic

Perm i a n

Fig. 3 Permian and Triassic data for marine families . The histogram shows the total number of families in each series, with the new families indicated by the cross-hatched symbol. The percentage extinction [calculated as percentage (total extinctions)/(initial diversity + total originations)] is shown above. Families whose originations or extinctions could not be resolved to series are not included. The graph at the top shows the ratio of originations to extinctions (OIE). The ratio falls below 1.0 during the Leonardian, begins to rise in the Induan, but does not climb above 1.0 until the Olenekian. A Asselian, S Sakmarian, L Leonardian, G Guadalupian, D Dzulfian, I Induan, 0 Olenekian, A Anisian, L Ladinian, C Carnian, N Norian, R Rhaetian. (Data from Sepkoski 1982.) =

=

=

=

=

=

=

=

=

=

=

=

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

2 The Evolutionary Process and the Fossil Record ,-------' 50 A

50

40 30

.�

c .� x QJ

C

.� '"

�

Cl.

.� QJ c

'0 0 Z

.�

10

25

o

B

400

•

Amphibians -

D

Rept i l e s

300 ...

200

.... ... ... ,' ...

,

,

,

, ,

,

.

1 00 80 60 40 20

1 00 0

Cb

C QJ

�

QJ Cl.

5

B

500

c 0

30 'E 20 � 15 '0 0 10 Z

QJ U

""6

c 0

x 20 �

c o

'"

"t3

A

5 l Pe r m i a n

G

D

0

A

l C Triassic

N

Fig . 4

Permian and Triassic extinctions in marine genera . A, Percentage extinction (calculated as in Fig . 3). B, Total number of generic extinctions . Cb = Carboniferous. Other abbreviations as in Fig. 3. (Data from Sepkoski 1986 . )

'" QJ .-

25

0

3) . This ratio i s 2 . 0 i n the Asselian, but falls l . 0 in the Leonardian and reaches a minimum of 0 . 1 in the Dzulfian. Extinctions exceed origi­ below

nations from the Leonardian onward . Note that

38 new families in the 9% origination rate for the stage; however, extinctions total 152 (32%), and 100 (31%)

originations continue, with Guadelupian or a

in the Dzulfian . Several authors have even argued

0

.�'" c

C

QJ

�

QJ Cl.

E 15 � '0 1 0 0

z

20

5 0 Permian

Fig .

"t c

Triassic

Fig. 5

Number of families and percentage extinction (calculated as in Fig . 3) per stage of the Permian and Triassic. A, Terrestrial plants . (Data from Knoll 1984 . ) B, Terrestrial amphibians ((lepospondyli and labyrinthodonts) and reptiles (captorhinomorphs, pelycosaurs, theraspids, and archosaurs) . (Data from Olson in Silver & Schultz 1982 . )

The fourth occurred a t the end o f the Triassic

2 . 1 3 . 5) and removed archosaurian reptiles Silver & Schultz 1 982) . R. Sloan dis­

that an 'extinction' never occurred but origination

(Section

rates were severely depressed . While originations

(Olson

did decline, this cannot explain a drop in familial

tinguished a more complex pattern of vertebrate

diversity of

54% .

in

extinction

episodes:

two

in

the

Sakmarian ­

Terrestrial vertebrates and plants experienced a

Leonardian, two in the Guadelupian, and six in the

series of extinctions and ecological replacements

Dzulfian . His analysis showed that the survivors

from

of each extinction had a higher percentage of mam­

the Early

Permian

through

the

Triassic

5) . Eighty-one per cent of amphibian families

malian characters and smaller body size than those

became extinct near the end of the Leonardian;

which became extinct . Sloan suggested that the

(Fig .

interestingly, most of these families first appeared

regular cycle of extinction and replacement was

during the preceding glaciation . A second extinction

caused by post-glacial climatic oscillations . Preser­

pulse at the close of the Permian primarily affected

vational quirks are apparent as well, for the magni­

theraspids, and was followed closely by a third

tude of the Late Permian -Early Triassic extinction

extinction episode at the close of the Lower Triassic .

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


o

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 .

>

z c.:

« u
o

C

> cc c.: LW I

IlJ

�

IlJ c..

Mammal - l i ke re p t i l e s

21 0 Fig. 1 The pattern of evolution of Triassic non-marine tetrapods, showing the extinction of major groups at the end of the Carnian stage . The dinosaurs, and other replacing groups, appear to have radiated only after the extinction event, thus suggesting an opportunistic replacement rather than one involving long-term competition . For abbreviations see the legend to Fig. 2. (After Benton 1988, by permission of Macmillan Magazines Ltd .)

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

.�

if>

20 E � 10 '0 c:i

z

0

'§ 1 0 c Q)

.Q U

.�Q) c


:_,AAII A��

0·7 '§

j

Q)

0·6

c 0 '';:; u C

0·5

H

�

�

Ammonoids

B L.

�

C

.�Q) 0·4 c 0 x

0·3

Q) tl.

0·2

!

Geological t i m e

(1 0 6 yrs)

Fig. 2 Triassic ammonoid families . A, Total diversity. B, Total extinction rates . C, Per-taxon extinction rates. The total extinction rates were calculated as the numbers of families dying out per million years, and the per-taxon extinction rates as the total extinction rate divided by the number of taxa at risk. The five highest per-taxon extinction rates (possible mass extinctions) are indicated with arrows . Diversity and extinction rate data were calculated by Triassic and earliest Jurassic substages (Scythian, Hettangian, Sinemurian), and by zones (Anisian -Norian) . The 'Rhaetian' stage is included in the Late Norian . Abbreviations: Ans Anisian, Crn Carnian, Het Hettangian, Lad Ladinian, L . Tr Lower Triassic, Nor Norian, Scy Scythian, Sin Sinemurian . The fossil is Ceratites . (After Benton 1986 .) =

=

=

=

=

=

=

=

(Fig . 4C) showed two similar peaks, with a slightly higher one in the Late Norian, and a lower one in the Camian . Present evidence points to as many as three Triassic extinction events: at the end of the Scythian, in the Middle to Late Camian, and at the Triassic ­ Jurassic boundary; none of these is clearly larger than either of the other two . The temporal spacings of the three events are as follows:

'"

.!':!

E � '0

cl Z

197

2 . 13 Mass Extinction : Events A

20 10

600 '" .!':!

0

�

'0

�

"

Total

0

A

500 400 300

B

c

240

230

220

21 0

15

B

200

Geological t i m e (1 06 yrs)

Triassic and earliest Jurassic non-marine tetrapod families. A , Total diversity. B, Total extinction rates. C, Per­ taxon extinction rates. The four highest total extinction rates (possible mass extinctions) are indicated with arrows. The time-scale is subdivided into informal 'substages', numbered 1 -20 in the Triassic. For abbreviations see the legend to Fig. 2. The fossil is Thecodontosaurus . (After Benton 1986 by permission from Macmillan Magazines Ltd. )

Fig. 3

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

o �-----6 '-5 .�

0 · 04 0 · 03

c

Q)

c '0 x

�

0 · 02 0 · 01

Q) 0..

O �---'--�----'---'--r21 0 200 220 230 G e o l o g i c a l t i m e ( 1 0 6 yrs)

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

Most other pelagic biota have been studied in less

/i: u .E .iJ 0::

Z �

« 0 z

'" 0:: '" e: :0

m

8

7

&

2-D

Z « f=

u �

I

tV>

« « �

0 ", c-

'" E (; Qj

"0

cL

�W w«

3-

o b: t--

� -'

-' w

e: .�

1:

::J

�I l "

0 "-

,',I

'" 0 "-

3

2

1

I " I I I

E (; Qj

1

'"""' 0 20 %

�

B

& ' 8 0%oPDB

Post K·T evo l u t i o n

-D

4

:J 01) :J

'" 13

S u rvivors

"0

cL

<

O 0 ·5 3

4

1 15

I

1

1

1

I

c

li' P II

.

"I 1

'

I

·

.' ?'

.

I •

1

"

25

U

er: L.O.J

""-

::J

e:

U

-'

Of)

?

-'

11

[I

::J

'" 'c .8 :E e: '" e:

? ? ? ?

?

I

I

I

•

II

. -

1

I

1 1 I: :1

!I� il

• 1

III I I .-. •

1 1

I I. I I 1

1

1

•

."1

I

A "

"

? ? ?

'" 'c '" Cl. E '"

1 1

�

I

If) ::J

tL.O.J er:

45

35

I

1.1

"' -' :E

::J

I

I

1

I .

25

,

JJ. m

.�'"

0 L.O.J U «

j

- - - Benthic A. acuta - P l a n k t i c fi n e fract i o n

0·5

2

6

o 25% i

'

1

I

1

I m e: .� e:

'"

0

Qj �

0 -'

t---;:.:;; '" '" :2:

Q;

c. c. :::>

8

10 &

4 2

2 4

0

11

? I

.

". ."

I 1 11 1 11 11 11 11 11 11 1 11 111 1

I

I

D

I .

111 1 11 111 1 1

1 0 ' 1 0 0 1 1 , . 1 I I 1,1 1 1 1

1 111 1

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

204

>'"
i=

'" w I-

if) :> 0 w u

i'! w

'" u

z

::!

z
Z
i= I <,!

'" Iif)
z Cl.

::!

Z

u Z
W YO M I N G

A L B E RTA

MONTANA

NEW M E X I CO

COLOR A D O

TROP I CA L

PA R A -

S U C C ES S I O N AL

POLAR

FOREST

RAIN

DECIDUOUS

L E AV E D

RAIN

®

� FERN

SPIKE

PARA -

TRO P I C A L

DRY

FO R E ST

D I NOSAUR

D EC I D U O U S

FOREST

FOREST

��r�E ��r�E ® ®Y ®� D I NOSAUR D I NOSAUR

SUBHUMI D

B R O A D L E AV E D FOR EST

BROAD

M E SOTH E R M A L

TROPICAL F O R E ST

I

;#"' fSEPRI KNE

POLAR

NOTOPHYLLOUS

B RO A D

E VE R G R E E N

L E AV E D

D EC I DU O U S F O R E ST

® Iridium - rich boundary cloy again indicating a major widespread event that triggered off wildfires . The cause of the wildfires is not the important issue, but whether or not there was a major change in plant life at this juncture (Fig . 1 ) . The evidence from terrestrial plants points to a sudden event at the Cretaceous- Tertiary boundary with wide­ spread forest fires . But the pattern of change across the boundary does not seem to involve much in the way of extinction; rather it seems to indicate a climatic change with an increase in seasonality and the concomitant change in the pattern of distri­ bution of vegetation zones . It is striking that in Alberta broad-leaved deciduous forests both above and below the boundary indicate a comparable climatic regime, whereas in New Mexico the sub­ tropical dry forest of the end-Cretaceous is replaced by tropical rain forest in the Tertiary (Fig. 1).

Fig. 1 Changes i n vegetation at the Cretaceous -Tertiary boundary. (After Wolfe & Upchurch 1986 . )

To r r e j o n i o n

z «

Z

« o

tpeciesl 10

I' " " "

,

,I ,I

11

i I

H e l l Creek Fig. 2 Changes in mammalian faunas across the Cretaceous- Tertiary boundary . (After Archibald & Clemens 1984, by permission from Macmillan Magazines Ltd . )

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

AGE Ma

U

E� Z �o N

STAGE

::; 64 -

TOR R EJON I A N

T K

P U E R CA N

Z
HELL CREEK F M .

Z

H O R S E SHOE

I ..J

Z :'! Z 0 I-

0 ::; 0 w

72 73 74 75 76 77

33

t Z :'! I I-

0

=>

...,

I

I I

/ L A N C E FM .

CA NYON

FM.

D I NOSAUR

P R OV I N C I A L PA R K , A L B E RTA

15

10

5

0

5

10

15

Diversity of dinosaur genera in the Upper Cretaceous showing the decline below the Cretaceous ­ Tertiary boundary . (After Sloan et al. 1986 . ) Fig. 3

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

AGE Ma

STAGE

C H E LO N I A �

EOSU C H I A ..-------,

I-- S Q U A M ATA ------l LAC E'3.T I L I A

SERPENTES ..-------,

11

CROCODY L l A �

PTERO S AU R I A �

� . ,

I

I I

I I

.

I I

I

I

:

ILl
a:: :::>
ILl
zo
ILl
:I: U :::> en :::> a:: :::>
I ILl
ILl
.J a:: >- :::> Cl U Cl

ILl
:I: U a::
LU
i=

Z 0 Cl 0 z
Changes in reptilian faunas across the Cretaceous -Tertiary boundary. (After SuIlivan 1987; Sloan et al. 1986 . [© copyright 1986 by the AAAS] . )

Fig. 4

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

D I N O SA U R I A

I

f------ S A U R I S C H I A ----f---- O R N I T H I S C H I A CO E L U ROSA U R I A

I

Cl> �

2

� o Cl> o

., �

�

C o "0 o

� 0 Cl> 0 c: c: 0

c

f;

Cl> ., Cl> -

� �

� o (f)

e "0 lJJ

�

� 0 0 .<: Cl> � c:

i [I� �

� 0

� g

� o Cl> o e o �

Cl>

�

Cl>

�I Cl> 01 �

Cl> �

Cl>

C E R ATO PS I A I I .------.. ANKYLOSAU R I A .------,

ORN I T HOPODA

lJJ
lJJ
a: :::;)
a: :::;)
�

>­ I-

'---

Cl>

o .<: Co ., U o u o

Q.

I- 0 I- 0 I- a. Cl Ul

� �

.=!

� lJJ lJJ
::;: o :I: IZ a: o

lJJ
lJJ
ii:

:::;)
�

�

:::;) a:


�

, ___J L______--'

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 .

C3 lJJ

:::;) a:

­ � Z
-'---'

L_ _

L_ _ ---'

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

Acinonyx [ A m e r i c a n c h e e ta h ) 8oother/urn [ tv\ u s k o x ) PI,}IVXOn H s ( Pe c c a r y ) >\rLfodus ( S h o rt - f a c e d b e a r )

1. 1

, !

I

I

I

1

Megafoll,vx I M e g a l o n yc h i d s l o t h ) Srock oceros [ P r o n g h o r n ) Cdpromer�'x ( P r o n g h o r n ) Mammufhus (Mammoth) .... . riops I S h a s t a s l o t h ) , 'othrulhe M a m m u t [American mastodon ) Cdme/ops ( C a m e l ) Equus [ H o r s e ) PJn th e ra [ A m e r i c a n l i o n ) Cervalces ( S t a g - m o o s e l

Cds rom ides I C i a n t beave r ) Glossotherium I M y l o d o n t s l o t h ) S m ilodon ( S a b re - t o o t h ( a t ) My/oh.vus ( l o n g - n o s e d p e c c a r y I Hemlduchenia ( L l a m a ) Eucera / ilCrlum ( S h r u b o x )

1 8000

55

==

=

Years B P

;

8000

Fig. 1 Terminal dates of some North American mammals based on reliable Carbon 14 dates. (Data from Mead & Meltzer in Martin & Klein 1984 . )

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

(CH20h o6 (NH3h 6 H3P04

+

H3P024

10602 :::;. 106C02

+

+

16NH3

+

1 06H20.

Thus, according to Avogadro's Principle, 1 mole (3 . 53 kg) of organic carbon requires 106 moles (2374.4 1) of oxygen. Decay rate is commonly ex­ pressed as a half-life . Since aerobic decay of 1 g of organic carbon requires 671 cm3 of oxygen, the oxygen demand for aerobic decomposition can be expressed

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

>­ « u L.U o

I�E�a_rl�Y

M I N E RA L I ZAT I O N

�

La --,

__ __ __ __ __ __ __ __ __ __ __ __ __ __

Fig. 1 The relationship between decay and mineralization in the preservation of soft-bodied and lightly skeletonized organisms . Reduced decay and early diagenetic mineralization are required for preservation of volatile tissues such as muscle. The preservational field of each tissue type extends from the bottom left-hand corner of the box to the boundary fence of the next most refractory type. (After Allison 1988 . )

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)

+

++

++

(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

t

b

-

� A

S t a b l e fa l l

B

U o ,, , b / ,

\�) �

"

,

" ' I

�_

.

j)

",

, -- - - ....... ,

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

R I V E R S , T I DAL STREAM S

�

U n ste dY fa l l

(1 -bla )

'

(1 - bla ) � o . 4 _____ _ __

(,.'

.

F

Turritella

L

. .

.

.

"

•

:.

Cerastoderma

�

__

H

K

E

• •

0 .4

' '� __�

__ __ __ __ __ __

WAVE ( O S C I L LATO RY) C U R R E NTS

,

�

/' I

... 1

Steady fa l l

__ __ __ __ __ __ __

Transport in one-way currents (rivers, tidal streams)

_ < : � w� "..::.� . _ . . . . . . . . .. .. . . . . . . . � � (�::��: {� . �

�.

S ETTL I N G

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 .

; :

: .. ! .: .. . : : :

. . .:

:: :

Mytilus

G

0

,

B e l e m n ite g u a r d s

Mytilus

S t r o n g c u rrents

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 .

=

=

=

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 . )

;;

o ;;:: '" Cl)

� .!!! C Q)

�

0...

.- -

,

75 50

"

,

- - - - Rhododendron s p . "

. . Fagus sylvatica

"

_ .

"

25

o

2

231

4

6

"

"

"-

"-

8

'-

- . - . - Alnus glu tinosa

.....

10

Days

12

14

16

- - -

18

20

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

2.6 mm

3.1

mm

S h eep m o l a r Ast raga l u s m ed i u m artiodactyl

( Oamaliscus)

Verteb ral cent r u m g i a n t forest h o g

( 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

CJ -

CJ -

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

=

=

. .

0· · · · .

. . . . ·.·...

·a.Q '

.

.

.

.

'

.

B i ogen i C

Sed i m entological

D i agenetic

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

C o m m u n i ty

I I

<=:J

death/ decay

�

b i o strat i n o m i c p rocesses/ti m e ave rag i n g

Q

T i m e-averaged asse m b lage

a

d i agen e s i s

F O S S I L AS S E M B LAG E Fig. 3 Relationship of the various kinds of assemblages and the processes which shape them.

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

·

�?." � ..

...

.

.

. . .� . . .-.t.:: . -� ... . 0 .. . . -� ..\�� - - - - - . . ·-.. ·. . · .-. . .. . .. .-. . A . . . .

.

.

.

.

.

·

�D

-

F

c

.

. .... ,

"

,-

"

.

"

.

�

�

G

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

""

'\

"

'.� G . �

,

\

�

t

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

/!

pe r m i n e r a l iza

�

3 Taphonomy O rgan i c ce l l wa l l

�e

B

Permineralization

SSion

'. f;8 ..

Pyr i t e , s i l i ca o r calcite

Pet r i fact i o n

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

268

3 Taphonomy

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

269

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

270

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

272 1 5 000

G e n e ra ( a l ive

A

+

dead)

1 4 000

1 0 000 I n d iv i d u a l s ( a l ive

B

+

dead)

9000

5000

-;u :J -0

'"

:�

-0 c

'0

o z

4000

I n d iv i d u a l s ( a l ive on ly)

3000

B i ovo l u me

2000

1 000

10

20

30

40

50

60

70

80

90

N o . of taxa

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

:::....- ....

-. ·'i..;>���:��:.���.;�::�<:� �.

-

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

,.

"

;,

. ..

of .

i� . "

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,,. � •.

... �.

" ',, :

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

" ....

._.!IIrJo

, � .:s:r: /

":::. ....

' � C ------j '

I"

·

�'�-------::::.--I

�-------l

"'" '/____ ___

�---'�'�-���� ' ...

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.

3 . 1 1 Fossil-Lagerstiitten

·

.

.

E III 6m

·

·

·

·

. .

. .

.

·

.

r ·

·

11

�I c: ()

!:: Ci5

'"

�

4m

E

11

12

:::J

�

V �

::

'"

� u <J)

H-H-t-L-j 'l.

2m

��!;�� .2.::;

E II 3 E I I 2 =F E ll 1 E!4

-

cg L i mesto n e � Mar!

�

CS

r--:",:- +---+---I . ", ---'-_ EI� 2 +--f--"-� +---+---1 :0 �

� - -F"-i E I 1 f-----'--

Bitu m i no u s sha!y marls � B i t u m i n o u s s h a !y m a r ! s w i t h sed i m e n t feed e r h o r i z o n s

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

high co n s u m pt i o n o f oxyg e n by d ecay

293

a n n u a l t u r n over

p o i so n i n g of lake­ I---;-� dwe l l i n g verteb rates

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