Advances in Botanical Research, Volume 16

Advances in

BOTANICAL RESEARCH VOLUME 16

Advances in

BOTANICAL RESEARCH Editor-in-Chief J. A. CALLOW

Editorial Board H. W. WOOLHOUSE W. D. P. STEWART

W. G . CHALONER E. A. C. MAcROBBIE

Advances in

BOTANICAL RESEARCH Edited bji

J. A. CALLOW

VOLUME 16

I989

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CONTRIBUTORS TO VOLUME 16

P. R . BELL, Deparlment of' Botcmj~ant1 Microbiology, University College, London U'CIE 6B7: U K J. L. HARWOOD, Deprirtrnent of' Biochemistry, University College, Cardif CFI IXL, UK P. M . HOLLIGAN, Murirw Biologid Association qf the U K , Cituriel Hill, Pljwiouth PLI 2PB, U K A . L. JONES, Depcirtment of' Biochemistry, ~Jnirvrsity College, Curdif CFI I X L . U K R . A . SPICEK. Dt>purtment of' Earth Sciences, IJniversity of Oxford, Parks Roud, O.yfiwdOX1 3PR. U K

This Page Intentionally Left Blank

PREFACE

This volume of A h w i c r s in Botunicul RoscurcIi contains articles on lipid metabolism in algae (Harwood and Jones), the alternation of generations (Bell). the formation and interpretation of plant fossil assemblages (Spicer) and primary productivity in the shelf seas of N W Europe (Holligan). Lipid metabolism in algae is extremely diverse which is not unexpected given the diverse evolutionary origins of the group. The review by Harwood and Jones considers the broad range of lipid structures and underlying metabolic processes found in the algae, biit concentrates on results of the relatively few detailed studies that have been made in genera of microalgae such as C 1 1 / u t ~ ~ ~ ~ t i o tDuti(ilidlu, ~ i o t i ~ . ~ . Atiuc:l:vris. and some of the ‘higher’ marine algae such as the fucoids. The relative paucity of detailed studics on algae suggests that further study will be rewarding in uncovering novel pathways that could be important in biotcchnological exploitation. The phenomenon of ‘alternation of generations’, or the change in phase coincident with meiosis, used to form the backbone of elementary botanical training. Unfortunately. its association with often uninspired teaching based on ‘types’ has probably led botanists largely to neglect advanced study of this basic and radical shift in plant development, and the scientific opportunities afforded by lower plants in which this change of phase can be most clearly observed. This situation may change as molecular biologists seek good ‘systems’ in which to study changes in gene-expression and associated triggers or signals. Certainly the morphological events associated with the haplophase/diplophase transition are amenable to analysis by the exciting new molecular technologies and, especially for those without training in classical botany, the article by Bell is a good, thought-provoking introduction to the whole subject of alternation of generations, its basic characteristics in a whole range of plant groups, the associated ultrastructural changes, and an outline of the very small amount of experimental work that has been done so far. ‘Taphonomy’ is the study of the processes of fossilization and is therefore of fundamental importance to the accurate interpretation of the fossil record, and the reconstruction of ancient communities and environments. It is a subject that is relatively new and requires highly integrated multidisciplinary approaches for most effective study. In his substantial review, Spicer considers the various types of fossilization process, and there is a particularly vii

...

Vlll

PREFACE

fascinating account of how recent volcanic eruptions, and especially the events of Mount Saint Helens in 1980, have provided excellent opportunities to observe the consequences of explosive vulcanism in shaping one aspect of the fossil record. The stability of the global environment is currently a ‘hot topic’ in science and accurate predictions of the dynamics of populations, relevant, for example, to the proper exploitation of biological resources and the control of environmental degradation, requires reliable estimates of the various processes leading to the exchange of materials in different components of the global ecosystem. In the final chapter of this volume, Holligan reviews understanding of the ecology and productivity of the important phytoplankton component of marine systems, specifically in the shelf seas of NW Europe. While much is known of the temporal and spatial aspects of phytoplankton growth and the physiological and environmental factors controlling it, less appears to be known about aspects of productivity and the flux of materials through phytoplankton. Holligan considers how improved methodologies and greater cognisance of the physical mixing process in tidally-stirred shelf seas will improve our understanding of productivity. Finally I would like to thank all the authors of articles in this volume for their patience with the editor and their efforts to make his task easier. J. A . CALLOW

CONTENTS

CONTRIBUTORS T O VOLUME 16. . . . . . . . . . .

V

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vii

PREFACE.

Lipid Metabolism in Algae JOHN L. HARWOOD and A. LESLEY JONES I. 11. 111.

Introduction .

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1

Lipid Structures .

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2

Lipid Composition of Algae . . . . . . . . . . . . . . A. Fatty Acids . . . . . . . . . . . . . . . . . . B. Lipid Classes . . . . . . . . . . . . . . . . .

5 5 9

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12

V . Metabolism of Lipids in Cyanobacteria (Blue-Green Algae)

. . .

13

Studies with Halotolerant and Halophilic Dunulirllu Species

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19

Metabolism in Marine Algae . . . . . . . . . . . . . . A. Labelling Characteristics . . . . . . . . . . . . . B. Positional Distribution ofAlgal Fatty Acids . . . . . . . C. EKccts of the Environment on Algal Lipid Metabolism. . . .

28 28 33

VIII. Lipid Metabolism in Other Algal Types . . . . . . . . . .

42

IV. General Remarks on Plant Lipid Metabolism

VI.

VII.

IX.

Conclusions

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35

47

The Alternation of Generations PETER R. BELL I.

Introduction . . . . . . . . . . . . . . . . . . .

11. The Universality of Life Cycles .

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ix

55 56

CONTENTS

X

I11 . Essential Features of Points of Change . . . . . . . . . . A . Gametogenesis . . . . . . . . . . . . . . . . . B. Sporogenesis . . . . . . . . . . . . . . . . .

57 57 65

IV . The Significant Features of Aberrant Cycles . . . . . . . . . A . Aberrant Cycles in Natural Conditions . . . . . . . . . B . Induced Aberrations in Sexual Cycles . . . . . . . . .

70 70 72

V . The Causal Approach to Alternation . . . A . General Assumptions . . . . . . B . From Gametophyte to Sporophyte in the C . From Sporophyte to Gametophyte . . VI . General Conclusion .

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. . . . . . . . Lower Plants . . . . . . . . . . .

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78 78 78 82 87

The Formation and Interpretation of Plant Fossil Assemblages ROBERT A . SPICER 1.

Introduction . . . . . . . . . . . . . . . . . . . A . The Quality of the Plant Fossil Record . . . . . . . . . B. Vegetational Heterogeneity . . . . . . . . . . . . .

96 98 100

I1 . Plant Remains as Sedimentary Particles . . . . . . . . . . A . Allochthonous and Autochthonous Assemblages . . . . . B . Settling Velocity . . . . . . . . . . . . . . . .

101 101

111. Aerial Dispersal andTransport ofplant Organs . . . . . . . A . Leaf Abscission . . . . . . . . . . . . . . . .

104 104 106

B.

Organ Dispersal by Wind

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103

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112

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114 115 119 122

VI . Fluvial Transport . . . . . . . . . . . . . . . . . A . Channel Deposits . . . . . . . . . . . . . . . .

125 126

VII . Lacustrine Environments . . . . . . . . . . . . . . . A . Fluvio-lacustrine Deltas . . . . . . . . . . . . . .

130 133

IV .

Litter Degradation o n the Forest Floor

V . Aquatic Processing of Plant Debris . A . Initial Processes-Floating . . B . Transport in the Water Column C . Lcaf Degradation . . . . .

VIII . Fluvio-marine Deltas and Estuaries . A . Pro-delta Slope . . . . . . B . Distributary Mouth Bars . . C . Tidal Flats . . . . . . . D . Interdistributary Embayments .

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140 141 142 143 144

xi

CONTENTS

E . Beaches . . . . . . . . . . . . . F . Lower Delta Plain Marshes . . . . . . . G . Upper Delta Plain Marshes . . . . . . . H . Deltaic Lacustrine and Fluvial Environments. I . Detrital I'cats . . . . . . . . . . .

IX .

Peat and Coal Assemblages

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147

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X . Vulcanism . . . . . . . . . . . . . . . . . . . A . The Importancc of Explosive Vulcanism to the Plant Fossil Record: Case Studies . . . . . . . . . . . . . B . Debris Flows . . . . . . . . . . . . . . . C . Preservation in Air-kill Tephra . . . . . . . . . 1) . Lateral Lakes in Volcanic Tcrrnins . . . . . . . . E . Post-eruption Vcgetation Recovery . . . . . . . . XI .

Prcservation and Diagcncsis . Conipt-cssion'lmpressions B . Duripartic Prcscrvation . C . Tissue Mineralization . D . Casts and Moulds . . . A.

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151

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152 160 166

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168

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172 175 175 176 I76 178

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179 1x0 180 1x1

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183

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184

XI1 . Applications of Plant Taphonomy to the Fossil Record . . . A . Specimen Morphology and Taxonomy . . . . . . . B . C om m it ni t y Reco 11s t r uc t i on . . . . . . . . . . C . Rcconstructing Community Suites a n d Regional Vegetation D . The llse of Plant Fossils in Sedimentology . . . . . . XI I I . Conclusions

i44 145 146 147 147

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Primary Productivity in the Shelf Seas of North-West Europe P . M . HOLLIGAN I.

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194

I1 . Ecological and Physiological Perspectives . . . . . . . . . . A . Ph y t o pla n k to 11 Distributions . . . . . . . . . . . . B . Control of Phytoplankton Production . . . . . . . . .

196 196 202

Ill.

Introduction .

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Methods for Estimating Primary Productivity A . Nutrient Budgets . . . . . . . . B . Oxygen and Carbon Fluxes . . . . . C . Biomass Distributions . . . . . . D . Primary Productivity Models . . . .

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IV . Environmental Conditions for Phytoplankton Growth in the NW European Shelf Scas . . . . . . . . . . . . . . . A . Mixing, Processes, Seasonal Stratification . . . . . . . . B. Light Availability . . . . . . . . . . . . . . . .

212 212 213 215 217 217 217 220

Lipid Metabolism in Algae

JOHN L. HARWOOD and A . LESLEY JONES

Dtpwtmeiit of' Biochemistry, University College CurdiflL CardiffCF1 I X L , U K

I. 11.

Introduction .

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.

Lipid Composition o f Algae. . . . . A. FattyAcids. . . . . . . . . B. Lipid Classes . . . . . . . .

IV.

General Remarks on Plant Lipid Metabolism .

v1.

VII.

VIII. IX.

i

2

Lipid Structures

Ill.

V.

. . . . . . . .

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

5 5 9

. .

12

. .

13

Studies with Halotolerant and Halophilic Dunuliellu Species . . . .

19

Metabolism in Marine Algae . . . . . . . . . . . . . A. Labelling Characteristics . . . . . . . . . . . . . B. Positional Distribution of Algal Fatty Acids . . . . . . . C. Effects of the Environment on Algal Lipid Metabolism . . .

. . . .

28 28 33 35

. . . . . .

42

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

47

Metabolism of Lipids in Cyanobacteria (Blue-Green Algae) . .

Lipid Metabolism in Other Algal Types . . . . . Conclusions .

.

. I.

INTRODUCTION

Algae are an extremely diverse group of organisms. Not surprisingly, thereAdvances in Botanical Research Vol. 16 ISBN 0-12-005916-9

Copyright $2 1989 Academic Press Limited All rights of reproduction on any form reserved.

2

J O H N L. H A R W O O D A N D A . LESLEY J O N E S

fore. their lipid composition and metabolism are exceptionally varied. In this chapter we have concentrated attention on groups of organisms which have been studied in reasonable detail. This selection has, in consequence, neglected some interesting, but isolated, studies. Nevertheless, we believe that it allows readers unfaniiliar with lipids to assimilate more useful information. I n any case. plenty of reviews dealing with specialized aspects are referenced. In order to lay a basis for further discussion of metabolism, we have begun with sections on lipid structure and occurrence in algae. The metabolic sections then deal with organisms of increasing complexity. from the primitive cyanobacteria to marine macroalgae. Finally. we end with a section devoted mainly to green algae, which can be regarded as the nearest in metabolic characteristics to higher plants.

11.

LIPID STRUCTURES

The complex lipids of plants are mainly amphiphilic molecules with a hydrophobic head group and a hydrophilic “tail”, enabling them to form the lipid bilayers of membranes. Algae contain many of the lipids found in higher plants, and also some unusual lipids. The basic structure is a glycerol backbone derived from glycerol 3-phosphate (from the photosynthetic Calvin cycle, or glycolysis) to which is esterified the hydrophobic head group. Phospholipids have phosphate esterified to the sn-3 position with further moieties esterified through this. Glycolipids have sugar moieties as a head group. The structures of the major phospholipids and glycolipids found in algae are given in Fig. 1. Most of the eukaryotic algae contain a range of phospholipids and glycolipids, many of which are found in higher plants. However, the prokaryotic cyanobacteria have only the lipids of the chloroplast thylakoids of higher plants: namely monogalactosyldiacylglycerol (MGDG), digalactosyldiacylglycerol (DGDG), sulphoquinovosyldiacylglycerol (SQDG) and phosphatidylglycerol (PG) (Fig. 2) (Gounaris e f al., 1986). Tri- and tetragalactosyldiacylglycerols have been found in some higher plants, and Chlorrllu contains trigalactosylglycerol (Benson e f al., 1958). Sugars other than galactose may be found. Some red algae have mannose and rhamnose in their glycolipids (Pettitt, T. R., Jones, A. L. and Harwood, J. L., unpublished). Monoglucosyldiaglycerol (MGlcDG) was found in Nostoe calcicnla (Feige et al., 1980) and Anuhaena variahilis (Sato and Murata, 1982a). In A . variuhilis, MGlcDG appeared to be a metabolic intermediate, being rapidly converted to MGDG by epimerization of C-4 of glucose (Section V). Pham-Quang and Laur (1976a,b,c) found a range of novel glycolipids, phospholipids and sulpholipids in three brown algae, Pelvetia canuliculufn, Fucus vesiculosus and F. serratus. The two Fucus spp. also contain one major

3

LIPID METABOLISM IN ALGAE

unknown lipid (Smith and Harwood, 1984a; Jones and Harwood, 1987). In C. c r i s p s and P. lunosa, 3SS-labellingrevealed a number of sulphur-containing lipids, most of which were minor components (Pettitt, T. R.. Jones, A. L. and Harwood, J. L., unpublished). However. one of these lipids was identified as phosphatidylsulphocholine (PSC), the sulphonium analogue of phosphatidylcholine (PC) (Fig. 3). which has also been identified in diatoms and a Euglena species (Anderson ct ul., 1978a,b; Bisseret L ’ t d.,1984).

ALlprd

X

PA

-H

PC

-Ct$CH2N(CH3)3

PE

+ -C H2C $N H3

PS

+ 4H2CHNHj

+

I

cooOH

OH

PI

PG

DPG

-CH

C$OC-R

I

I

I

0Fig. I . Structures of common phosphoglycerides. PC, phosphatidylcholine; PI, phosphatidylinositol; PE, phosphatidylethanolamine; PG, phosphatidylglycerol; PA, phosphatidic acid. Based on Harwood and Russell (1984).

4

JOHN L. HARWOOD A N D A. LESLEY JONES

Chlorosulpholipids have also been found in some algae and are a major component of Ochromonas danica (Elovson and Vagelos, 1969). An unusual lipid found in a number of green algae and some lower plants, but not detected in angiosperms, is the homoserine ether lipid 1(3),2-diacylglyceryl-(3)-O-4'-(N,N,N-trimethyl)-homoserine (DGTS) (Fig. 4), first identified in 0. danica (Brown and Elovson, 1974). This lipid has since been

X -

Lipid

MGDG

DGDG

?H

I

SQ DG

CH20H

C H2-S Fig. 2 . Structures of common glycosylglycerides.

4-

LIPID METABOLISM IN ALGAE

5

0Fig. 3 . Structure of the sulphonium analoguc ofphosphatidylcholinc

Fig. 4. Diacylglycerol trimethylhomoserine ether lipid. identified in Chlumydomonus reinhurdtii, Dunuliellu sulina, Codium spp., Ulvu pertusu and Enteromorphu intestinalis (Sato and Furuya, 1984a,b), and is a major lipid of Chlumydomonus reinhurcitii and D. sulinu (Eichenberger, 1982; Norman and Thompson, l985b). Algae also contain neutral lipids, mostly as triacylglycerols which are, presumably, storage products (Pohl and Zurheide, 1979a,b) with small amounts of mono- and diacylglycerols. They also contain various hydrocarbons as minor constituents and a range of sterols and sterol esters (see Pohl and Zurheide, 1979a). Thus the range of lipid structures in algae varies from the simple constituents of the cyanobacteria to the complex variety in the eukaryotic brown (and other) algae. The structures found vary between the algal divisions and some lipids appear to be characteristic of different algal divisions-for instance, DGTS is found in many Chlorophyceae but has never been detected in any Phaeophyceae. The distribution of lipids within different algae is considered in more detail in the following section.

111.

LIPID COMPOSITION OF ALGAE A. FATTY ACIDS

A large number of algae have now been analysed for their fatty acyl composition. The convenience and sensitivity of gas-liquid chromatographic

6

J O H N L. H A R W O O D A N D A . LESLEY JONES

(GLC) methods have made this possible, whereas, in contrast. there has been much less work on the content of individual lipid classes in either marine or fresh-water algae. Fresh-water algae typically contain similar fatty acids to terrestrial plants. However, the proportions of such acids differ considerably from, for example, higher plant leaves. In general, even-chain acids in the range C,,C,, account for the bulk of the components. In contrast to plant leaves, fresh-water algae usually have a relatively high proportion of C , , fatty acids and reduced levels of C, unsaturatcd fatty acids, especially r-linolenate (Harwood rt d.. 1989). Of course, the total fatty acid composition of organisms gives little information about the specific acyl contents of individual complex lipids, which are usually very different. For example, it has been noted by several authors that triacylglycerols that can accumulate in certain species of algae are usually very low in polyunsaturated fatty acids (e.g. Tornabene ('I u/.. 1983). in contrast to total algal extracts (see Hitchcock and Nichols, 1971). Furthermore, in an analysis of the individual lipids of two strains of Chlam?.doomotiu.F rc.inhardtii. Eichenberger et ul. (1986) noted that. whereas the glycosylglycerides. PG and phosphatidylinositol (PI) contain mainly or exclusively the n-3 isomer of linolenic acid, phosphatidylethanolamine (PE) and DGTS contained the 11-6isomer (1'-linolenate). I n addition, it should be remembered that environmental factors such as light, temperature, nitrogen levels. salt stress or pollution can have a marked effect on fatty acid (and lipid) composition. Representative fatty acid compositions of some fresh-water and salttolerant algae are given in Table I. It will be seen that whereas the C, fatty acids are absent (or only found in trace amounts) in fresh-water algae, these acids may be significant components of organisms living in high-salt environments such as the Dead Sea. In fact, for marine algae the very long chain polyunsaturated fatty acids arachidonic acid and eicosapentaenoic acid (n-3) are usually major components (Pohl and Zurheide. 1979a; Harwood r t al., 1989). Marine algae in general contain a bewildering array of major fatty acids. Some representative examples of compositions for phytoplankton and macroalgae are shown in Table TI. Palmitate is, invariably, the major saturated fatty acid of phytoplankton with myristate often being found in appreciable quantities. In contrast to higher plants, C,, fatty acids are less important, with palmitoleic acid being the major monoenoic acid component. In some cases, e.g. Monochrysis lathrri (Table 11), total C,, acids represent a very minor proportion of the total acyl constituents. One common theme for all marine algae, with the exception of the Chlorophyceae, is that C, polyenoic acids are major constituents. Arachidonic and eicosapentaenoic ( n - 3 ) acids are the main C,, acids and sometimes represent a very high proportion of the total acyl groups of particular lipids. For example, in F. serratus arachidonate accounted for 67% of PC (Smith and

7

L I P I D M E T A B O L I S M IN A L G A E

F a t t y acid composition (“A, total)

16:O 16: I 16:2 l h : 3 16:4 18: I 18:2 I X : 3 1X:4 3 0 : s 3 2 : h F r e s h w a t c r spp.

Scene~1rsniu.sohliquus 35 Clik>r~llti vulguris 26 Chumy1onionu.s 20 reitiliurdt ii S a l t - t o l e r a n t spp. Anki.st,otli~.sriiusspp. I.socI1r:v.vis spp. Nuiinoclrliwi.r spp.

13

3 8 4

tr.

tr.

15

7

2

-

9 2

1

4

23

7

1

14 15 -

25

I

3

12 6 9 2 0

~

~~

7

9

4 4

6 34 6

30 20

2

30

3

2 6 1

29 17

2

~

I - -

1

2 27

-

13 ~~

Data from Hitchcock and Nichols (19711, Hen-Amotz and Tornabene (198.5) and Eichenberger el t i / . (1986). Fatty acids are abbreviated with the figure before the colciii indicatinp tlic number of carbon atoms. and the figure alter the colon indicating the number of double bonds contained.

Harwood, 1984a). while in Chondrus crispus eicosapentaenoate represented more than 25% of the total acids of the glycosylglycerides (Pettitt c ~ tul., 1989). The unicellular marine alga Chnrtonclla untiyuu (Raphidophyccac) was also found to contain rather higher amounts of eicosapentaenoate in all lipid classes (Sato er a/., 1987). A very unusual fatty acid which is found in photosynthetic tissues From higher plants is truns-A3-hexadecenoate. This acid is locatcd exclusively at the sn-2 position of PG (Harwood, 1980a). Interestingly. in view of the postulates concerning its possible role in granal stacking (see Bolton et d., 1978). the same acid is also found in PG in algae with quite different chloroplast morphology. Thus, it has been reported in brown algae (Smith and Harwood, 1983), red algae (Pettitt and Harwood, 1986), Raphidophyceae (Sato et a/., 1987) and diatoms (Kawaguchi er al., 1987). Together with all the negative evidence from higher plants (Bolton er d.,1978), it is clear that whatever the role truns-A3-hexadecenoate plays in nature, it is not in granal stacking. More likely explanations concern its possible involvement with chlorophyll-protein complexes (Remy er al. 1982), as suggested by modelbuilding experiments (Foley and Harwood, 1982; see Foley er ul., 1988). Cyanobacteria, as an evolutionarily less advanced “algal” group, also contain much more simple lipid and fatty acid compositions than other algae. Murata and Nishida (1987) have divided cyanobacteria into four groups based on the original classifications of Kenyon et al. (1972). Examples of each of these four groups are shown in Table I l l . Strains in the first group contain only saturated and mono-unsaturated fatty acids, while those in the other three groups contain linoleate plus polyunsaturated acids characteristic

Fatty acid composition ( "/o total) 14:O 16:O 16:1

Phytoplankton Monochrysis lutheri (Chrysophyccac) Olisthodiscus spp. (Xanthophyceae) Lauderiu borealis (Bacillariophyceae) Amphiciinium carterue (Dinophyceae) Dunaliellu sulinu (Chlorophyceae) Hemiselmis hrutiescens (Cryptophyceac) Macroalgae Fucus vesiculosus (Phaeophyceae) Chondrus crispus (Rhodophyceae) U l w luctuca (Chlorophyccae) Fatty acid abbreviations as for Table I

10 X

16:2

13 14

22 10

5 2

16:3 16:4 7 2 12 tr.

18:l

I I

3 4

4

7

12

21

3

3 tr.

24

1

41

--

-

1

13

IS 3

1 tr.

3

tr.

tr.

2

tr.

26

-

21 34

1

18

-

2 6 2

tr. tr. tr.

~

-

1

1 ~

-

18

18:2

2 5 11

9 9

I t 6 1 1 8 tr.

18:3

18:4

2 8

r .

1 tr. 2 1 1 9

20:4 20:s 1

~~

5 -

1

8

2 1 9 1 3 -

-

9

30

tr.

10 1

7

4

IS

1

4

18

2

17

24

I

14 14

8 22 2

22:6 7 2

25 -

-

tr.

9

LIPID METABOLISM IN ALGAE

Group

1

2 3 4

Fatty acid composition ('YO total)

Organism

Anrrcj~.stisnidu1rti.s Atiuhicctm vrrriuhilis Sjnechoiystis 67 14 To1jpotliri.u tenuis

46 32 28 22

46 22 4 3

3 I1 5 16

0 17 17 15

0 16

0 6

0 0 3i 13

0 0 0 II

Data taken from Murata and Nishida (19x7). where rel'crences will he found. €.'ally acid ahhrovations as for Table I .

of each group. Thus, groups 2, 3 and 4 contain a-linolenate, ;j-linolenate and octadecatetraenoate (n-3), respectively (Table I1 1). Filamentous blue-green algae are distributed throughout the four groups, while the prokaryotic green alga Prochloron has a fatty acyl composition placing i t in the first group (Kenrick er d., 1984). B.

LIPID CLASSES

Just as the cyanobacteria contain a relatively simple fatty acid composition, so is their lipid content confined to four major classes only-monogalactosyldiacylglycerol (MGDG), digalactosyldiacylglycerol (DCDG), sulphoquinovosyldiacylglycerol (SQDG) and phosphatidylglycerol (PG). A minor lipid, monoglucosyldiacylglycerol (MClcDG), accounts for a trace amount in some species such as Anucysris vuriahilis but not in others (e.g. Anucystik niduluns). This minor lipid is involved in the biosynthesis of MGDG (see later). The lipid compositions of two cyanobacteria and Prochloron spp. are given in Table IV. When individual membrane fractions were isolated from Anacystis niduluns, the thylakoid, plasma and outer membrane all contained a rather similar amount of the four lipids except that DGDG was somewhat enriched in the outer membrane. However, the lipid content as a percentage of the dry weight was very different, being 57%, 19% and 3% for the plasma, thylakoid and outer membranes, respectively (Murata and Nishida, 1987). In nitrogen-fixing cyanobacteria unusual glycolipids have been reported. These are found i n the heterocysts of the filamentous heterocystous strains as well as in unicellular strains. In A . cylindricu, the glycolipids account for 4.4% of the total lipids. The chemical structures of the four main nonsaponifiable glycolipids were determined about 15 years ago (Bryce e t al., 1972; Lambein and Wolk, 1973) and other minor variants have been reported (see Murata and Nishida, 1987). Eukaryotic algae contain a formidable range of acyl lipids. As a general-

I0

J O H N L. H A R W O O D A N D A. LESLEY JONES

Lipid (YOtotal)

Organism

..IIItrhrrefltr L'oric/hi/i.s

nitluluti.s Proc~/l/ororlspp. A n i i ~ ' j . .tis \

MGDG

MGlcDG

DGDG

SQDG

PG

54 57

I 1i.m.

17 11 II

II II 26

21 5

_5 T_

3

17

not measured. Data takcn from Muratu a n d Nishida ( 19x7). where the original references can be found.

ii.ni. =

ization, the three glycosylglycerides (MGDG, D G D G and SQDG) are major constituents. So far as phosphoglycerides are concerned. all the main classes can usually be detected. Insufficient data are available for generalizations to be made but it appears, thus far, that there are considerable differences between algal divisions in their relative contents of individual phospholipids. Some examples of lipid compositions are given in Table V. DGTS is an unusual lipid which is found in the Chlorophyta, although it was first reported in the chromophyte 0. (lunicu (Nichols and Appleby, 1969; Brown and Elovson, 1974). I t represents a major component in green algae such as Ch1rini~~tlot~iotiu.v rrinhurcltii (Eichenberger and Boschetti, 1978; Table V). and a survey of its occurrence in non-vascular green plants has been made (Sato and Furuya, 1985). Apart from 0. dunicu, Chuttonrllu untiyuu (Sato r t ul., 1987: Table V) is the only chromophyte known to contain DGTS. The lipid has not been reported in brown algae (e.g. Smith and Harwood, 1984a) or diatoms (e.g. Kawaguchi P / ul., 1987). Many fresh-water algae contain chlorosulpholipids (Mercer and Davies, 1979). Again, it was work with 0. dunicu which first revealed large amounts of these lipids (Haines and Block, 1962). The substances were soon identified as sulphur esters that were present in amounts greater than for most glycolipids or phospholipids in the cell. Many of the sulphur esters also contain chlorine, and are therefore known as chlorosulpholipids. In 0. dunicu they represent about 15% of the total lipids. They have been detected in all freshwater species but not in any of the marine species examined (Mercer and Davies, 1979).These unusual lipids have been reviewed (Haines, 1973a,b). Certain diatoms have been found to contain other novel sulphur-containing lipids (Kates, 1987). Characteristically, all species examined contain three sulpholipids in addition to SQDG. They have been identified in Nitzchiu ulhu as sterol sulphate, deoxyceramide sulphonic acid and the PC analogue PSC (Anderson rt ul., 1978a,b; Kates rt ul., 1978). In the non-photosynthetic diatom N. albu, PSC completely replaced PC, but in other diatoms both lipids occurrcd together (Kates, 1987). Overall, the sulpholipids are major constituents of diatoms, representing 30Y0 of the total polar lipids in N. pelliculnsu

TABLE V Tlw acjl lipid conipositiotis Lipid ( O h ) PC PE PI PG DPG Other phospholipids MGDG

DGDG SQDG Other glycolipids DGTS Lipid X Neutral lipids Free fatty acids

Chatronella antiqud

Dutiuliella parvu

Aceiahulnriu meditarraticw ‘

9 n.d. 2 6

0.1 I .2 0.6 3

__

29 18 29 ~

6

of .sonic

ulgue

Chlat?i~.clot?ioti~i.s reiniiurdiiid

31 20 20

3

10

4.2’ 6.2 2.9

.-

37

A_-

5.4 ~

41 16 7

16.9 14.8 15.5

15.0 11.3 22.0

16

n.d.

n.d. 24. I 4.9

-

~

20

Fucus wsicuIosusJ

30.1 1 .5 trace 1.1 1.9

5

~

21 11 7 1 15

CIlOt1dr us crispus ‘’

-

~

3.4 2.2

I5 13

“Sato et ul. (1987); bKates (1987); ‘Eichenberger and Gerber (1987); dEichenberger et ul. (1986); ‘Pettitt n.d. = not detected.

el

ul. (1988b); ’Unpublished data

12

JOHN L. HARWOOD AND A. LESLEY JONES

and over 74% in N . alba. PSC has also been detected in marine red algae such as Chondrus crispus and Polysiphonia lanosa (Pettitt et al., 1988b). A review of the lipids of marine algae has been made by Pohl and Zurheide (1979a). There have been sporadic reports of a wide range of unusual structures. However, in many cases these have not been confirmed and may, in at least some cases, be the products of lipid degradation or modification during analysis. Such processes are well known in plant tissues, and special precautions must be taken to prevent their occurrence (see Harwood, 1980a).

IV. GENERAL REMARKS ON PLANT LIPID METABOLISM A detailed discussion of plant lipid synthesis is beyond the scope of this chapter, and, moreover, specific algal aspects will be dealt with later. However, a few very general remarks together with comprehensive references will be made here. Fatty acid metabolism has been reviewed very recently (Harwood, 1988). De novo synthesis involves the concerted action of acetyl-CoA carboxylase and a type I1 (dissociable) fatty acid synthetase. The end-product of such synthesis is palmitoyl-ACP, which can be specifically chain-lengthened to stearoyl-ACP using a special condensing enzyme. Thus C,, and C,, saturated fatty acids are the products of de novo synthesis. The first unsaturated bond is usually introduced at the A9-position by a desaturase which probably uses acyl-ACP substrates in most instances. Palmitoleic and oleic acids result from this action. Further desaturations are thought to involve complex lipid substrates such as PC and MGDG (Harwood, 1988). These may take place within choroplasts (prokaryotic pathways) or include extra-chloroplastic (eukaryotic pathway) enzymes. Fatty acids can also be elongated, and such reactions are clearly of great importance to many algae where C,, fatty acids are major constituents. Nothing is known about the substrates for such reactions in algae, although acyl-CoAs are used in a number of higher plant tissues (Harwood, 1988). Obviously, where both chain elongation and desaturation are involved in the formation of a given fatty acid, there will be more than one possible route. Thus, arachidonate has been shown in some algae to be formed by a desaturation-elongation-desaturation route from linoleate (Nichols and Appleby, 1969): 18 : 2 (n-6)+18 : 3 (n-6)+20 : 3 (n-6)+20 : 4 (n-6) In contrast, in a euglenoid (Hulanicka et al., 1964) it appears to be formed thus: 18 : 2 (n-6)+20 : 2 (n-6)+20 : 3 (n-6)+20 :4 (n-6)

LIPID METABOLISM IN ALGAE

13

So far as complex lipids are concerned, the formation of MGDG and DGDG (Joyard and Douce, 1987), SQDG (Harwood, 1980b; Mudd and Kleppinger-Sparace, 1987) and phospholipids (Moore, 1982; Harwood 1989) has been reviewed. The metabolism of unusual lipids such as the sulpholipids of diatoms (see Kates, 1987). chlorosulpholipids (Mercer et d.,1374) and DGTS (see Schlapfer and Eichenberger, 1983) has also been discussed. In addition, the arsenic lipid (arsenoribosylphosphatidylglycerol) which appears to mediate arsenic excretion in marine organisms has been discussed (Benson, 1987). Other general aspects of plant lipid metabolism will be found in the excellent volumes edited by Stumpf (Stumpf and Conn, 1980, 1987).

V.

METABOLISM OF LIPIDS IN CYANOBACTERIA (BLUE- GREEN ALGAE)

The cyanobacteria, like the eukaryotic algae, have an oxygen-evolving photosynthetic mechanism, yet their prokaryotic morphology makes study of their metabolism much simpler. Their lipid composition and metabolism have been recently covered in an excellent review (Murata and Nishida, 1987), so only a few aspects will be dealt with here. The plasma and thylakoid membranes of cyanobacteria contain glycerolipids-almost exclusively MGDG, DGDG, SQDG and PG. The outer membrane contains lipopolysaccharides and hydrocarbons in addition to glycerolipids. In addition, some nitrogen-fixing species of filamentous cyanobacteria may contain vegetative cells which change into heterocysts (Haselkorn, 1978). These heterocysts contain a refractile multilayered heterocyst envelope which contains unique glycolipids (glycosidic glycolipids and glycosyl ester glycolipids) (Lambein and Wolk, 1973). The glycerolipid composition of several species of cyanobacteria is shown in Table IV. It is noteworthy that the only glycerolipids present in appreciable amounts are those which are regarded traditionally as typical chloroplast thylakoid lipids (Harwood, 1980a; Gounaris rt d.,1986). In addition, it will be seen that for Anucysfis nzduluns, where more detailed analyses have been undertaken, the lipid compositions of different membranes in the cyanobacterium are broadly similar. However, the lipid contents (YO dry weight) are quite different, being 19%, 57% and 3% for the thykaloid, plasma and outer membranes, respectively (Murata and Nishida, 1987). In addition to the four main lipid classes present in cyanobacterial membranes, MGlcDG seems to be a ubiquitous, though minor, component (Feige, 1978). When the fatty acids of cyanobacterial lipids were first studied, it was realized that although these were broadly similar to those of higher plant chloroplasts, there were some notable differences. These include the increased

14

JOHN L. HARWOOD AND A. LESLEY JONES

,

importance of C (especially palmitoleic) acids, the relative reduced prevalence of polyunsaturated fatty acids (including the absence of linoleate and alinolenate from some organisms), the presence of y-linolenate in some cyanobacteria and an absence of trans-A3-hexadecenoate from PG (Hitchcock and Nichols, 1971; Murata and Nishida, 1987). Some efforts have been made to classify cyanobacteria into four subgroups, according to their fatty acyl composition (Kenyon, 1972; Kenyon et al., 1972) (see Section 111). Examples of fatty acid compositions for different organisms are given in Table 111. The individual glycerolipids differ from one another in their acyl compositions. In general, MGDG and DGDG contain the highest ratios of unsaturated to saturated acids. In those cyanobacteria which contain polyunsaturated fatty acids, the latter are also enriched in the glycosylglycerides. The two acidic glycerolipids, SQDG and PG, tend to contain very large amounts of palmitate with only small quantities of palmitoleate. Naturally, the fatty acyl compositions of cyanobacteria and their glycerolipids are very dependent on growth temperature (see later). All glycerolipids of cyanobacteria display the typical "prokaryotic" positional concentration of C,, acids at the sn-1 position and C , , acids at the sn-2 position (Zepke et al., 1978). Studies using ['"C] acetate first established the rapid labelling of all major glycerolipid classes (Nichols, 1968). When H14C0, was used for pulselabelling of 30 species of cyanobacteria, the first lipid highly labelled was MGlcDG. Later, radioactivity appeared in MGDG, and it was proposed that these lipids had a precursor-product relationship (Feige et al., 1980). Moreover, analysis of the glucose and galactose moieties of these two lipids in Anacystis nidulans showed a similar relationship (Fig. 5) and indicated that the sugar moiety was not lost during this interconversion. As a result of these experiments, Sat0 and Murata (l982a) proposed that the mechanism of formation of MGDG involved epimerization at the C-4 atom of the precursor glucose unit. In addition, experiments with cerulenin (see below) suggested that DGDG was formed by galactosylation of MGDG rather than via a glycolipid : glycolipid transferase (see Joyard and Douce, 1987). Cerulenin, a known inhibitor of fatty acid biosynthesis, was tested with Anacystis nidulans. Its inclusion reduced severely the incorporation of radioactivity from H1"C03 into all lipid classes except D GDG (Sato and Murata, 1982a). This was in keeping with the idea that newly synthesized acyl chains are needed for the overall formation of glycerolipids, but because DGDG can be synthesized by galactosylation of MGDG, its labelling is less affected. Indeed, analysis of the sugar residues of D G D G confirmed that a high proportion of the total radioactivity of this lipid was present in the galactose moieties (Sato and Murata, 1982a). A membrane-bound UDP-glucose : diacylglycerol glucosyl transferase was detected in A . variubilis (Sato and Murata, 1982a). This enzyme seems to be present in both thylakoid and plasma membranes (Omata and Murata, 1986) and it is interesting that, in higher plants, the equivalent galactosyl

LIPID METABOLISM IN ALGAE

I

15

r

Time ( h ) after labelling

(a)

(b)

Fig. 5. Changes in the radioactivity of monoglucosyl- and monogalactosyldiacylglycerol during pulse-labelling from HI4CO, in A . niduluns and subsequent chase. Gal, galactose; Glc, glucose. Taken from Sato and Murata (1982a)with permission. transferase is found in the chloroplast envelope and, in some cases, also in prothylakoids (see Murata and Nishida, 1987). Fatty acid synthesis was followed in A . vuriubilis by labelling from H14C03 (Sato and Murata, 1982b). Radioactivity was incorporated initially into palmitate, stearate and oleate. In fact, it was suggested that saturated fatty acids were initially incorporated into complex lipids such as MGlcDG and that subsequent desaturations occurred while the acyl groups remained attached to complex lipids. This was in agreement with proposals for higher plants (see Harwood, 1988). Examination of molecular species labelling of individual lipid classes led to proposals that in MGlcDG, stearate could be desaturated to oleate and linoleate but hardly at all to linolenate. In contrast, MGDG was an efficient substrate for successive desaturation of stearate through to linolenate as well as for that of palmitate to hexadecadienoate. DGDG did not appear to be used for desaturation, whereas successive desaturation of stearate, but not of palmitate, appeared to occur on PG and SQDG (Fig. 6). Direct demonstration of lipid-linked desaturation of palmitate in MGDG was made by the use of isotopic labelling. Incubation of cells with H13C03 caused the formation of MGDG enriched in its acyl groups. After 2.5 h, 19% of the palmitate but virtually none of the palmitoleate at the sn-2 positions were enriched in 13C. During a subsequent incubation for 7.5 h in the presence of unlabelled CO, and the fatty acid synthesis inhibitor cerulenin,

16

JOHN L. HARWOOD A N D A. LESLEY JONES

38°C

22°C

18:O 16:O [Gal

1

1

18:l 16:l [Gal

--+

E

18:2

GalDG

--+

18:l 16:O [Gal

- -1

18:3 16:O

18:Z

18:3 16:l

18:2

16:O

[Gal

L

[g;: -[

1611 Gal

Gal

1

Gal

18:3 16:2 Gal

I

1

1

I

I

J

Fig. 6. Pathways for the desaturation of fatty acids esterified to the acyl lipids of A . niduluns. Taken from Sato and Murata (1982b) with permission.

[I3C]palmitate was desaturated to [13C]palmitoleate.Mass spectrometric analysis of the 2-acylglycerol moiety showed that [L3C]palmitoyl[ I 3C]glycerol was converted to [ 3C]palmitoleoyl-['3C]glycerol, and ['ZC]palmitoyl-['zC]glycerol to ['ZC]palmitoleoyl-['ZC]glycerol. If a pathway involving deacylation, desaturation and reacylation had been involved, then this would have been expected to yield products containing partial enrichment (Fig. 7) and this was not found. The results were fully in support of an MGDG-linked desaturation of palmitate (Sato et al., 1986). The idea that desaturation of fatty acids in cyanobacteria required lipidlinked substrates was in agreement with data for A . variahilis reported by Lem and Stumpf (1984a). They showed that cell-free extracts were able to synthesize palmitate and stearate but not oleate from [14C]malonyl-CoA.In addition, although [14C]palmitoyl-ACPcould be elongated to ['4C]stearoylACP, n o desaturation was detected. When ['4C]stearoyl-ACP was used as

LIPID METABOLISM IN ALGAE

17

Lipid- linked desaturation

Gly ( U 1-16; 0 ( U) Gly (E)-16:0 ( E l

Gly(U )-16 : 1(U 1 Deacylat ion desaturation and reacylatton

Gly( E 1-16 : 1 ( U )

Fig. 7. Principle of isotopic species analysis to discriminate between the two possible mechanisms of dcsaturation of palmitate. Combinations of the glycerol backbone and the C16 acids at the sn-2 positions of MGDG are presented as Gly-16:O and Gly-16:I. U, unenriched; E. enriched with I T . Redrawn from Sato rt ul. (1986) with permission.

substrate in a A9-desaturase assay, activity was detected in green algae such as C. pyrenoidom, Scenedesmus ohliquus and Chlamydomonas moewensii, but not in A . variahilis or Nostoc spp. Data from other laboratories agree with the above conclusions (Stapleton and Jaworski, 1984b; Al Araji and Walton, 1980). The fatty acid synthetase of A . variahilis is of the type I1 non-associated type (see Harwood, 1988). The malonyl-CoA : ACP transacylase has been purified and found to have rather similar properties to that from spinach chloroplasts (Stapleton and Jaworski, 1984a). The elongation of palmitate to stearate uses palmitoyl-ACP and NADPH and not palmitoyl-CoA or NADH (Lem and Stumpf, 1984a; Stapleton and Jaworski, 1984a). Radioactivity from ['4C]acyl-ACPs was rapidly transferred into complex lipids, especially MGDG, by crude cell extracts of A . variahilis. The first intermediate detected was diacylglycerol (Lem and Stumpf, 1984b), but one presumes that the incorporation into this compound was due to glycerol 3-phosphate acylation and phosphatidate phosphatase. Acyl-CoAs could not act as substrates. Although [14C]oleoyl-ACPwas effective for acylation, the probable lack of formation of this compound in vivo (see above) would prevent the esterification of this moiety which would have to be formed by lipid-linked desaturation (Sato and Murata, 1982b). Compositional studies on cyanobacteria have demonstrated that shifts in growth temperature lead to several types of changes in lipids. In Anacystis

18

JOHN 1.. HARWOOD A N D A . LESLEY JONES

TABLE VI Chunge~in the moleculur .species composition qf’glycerolipids 0f’Anabaena variabilis c u u s t d by growth ietnperuture Lipid

Growth temp. ( C)

Molecular species (YOtotal) C-l C-2

GlcDG MGDG

DGDG PG

SQDG

38 22

18.0 1 8 . 1 1 8 . 2 1 8 : 3 1 8 . 1 1 8 : 2 1 8 . 3 1 8 . 3 1 6 . 0 1 6 . 0 1 6 . 0 16:O 16.1 16.1 1 6 . 1 1 6 . 2

24 22

60 40

10 24

38

1

25

22

2

2

23 12

38 22

1 1

16 4

24 20

0 19

1

56 10

41 26

48 10

26 16

sx

38

...77

0

38 22

10

2

0 6

0 0

0 0

0 0

0 0

1

11

34

0

35 3

0 32

0 12

16 I

38

0 0 3 1 4

0 61

0 0

0 0

0 0

0 0

0

0 0

0 0

0 0

0 0

9

Fatty acid abbreviations as in Table I . Taken from Murata (1987). with perinission

niciuluns, lowering growth temperature led to an increase in unsaturation and a shortening of chain length (Holton et a/., 1964). Similar changes were found with S~~nec.hococcu.s cedrorum (Sherman, 1979), and in S. lividus lowtemperature growth led to a decrease in palmitate and oleate and an increase of palmitoleate in MGDG and DGDG while stearate decreased and palmitoleate and oleate increased in PG and SQDG (Fork et ul., 1979). In Anucjxtis nidulrms, lowering growth temperature led to a decrease in chain length of mono-unsaturated acids at the sn-I position of all lipids but increased desaturation of palmitate at the sn-2 position of MGDG and D GDG (Sato et d., 1979). In contrast to the above, the unicellular cyanobacterium A . variahilis contains polyunsaturated fatty acids. Lowered growth temperatures led to an increase in a-linolenate at the sn-l position of all lipids, while the composition of C, acids at the sn-2 position remained nearly constant apart from a slight increase in hexadecadienoate in MGDG and DGD G (Sato et al., 1979; Sat0 and Murata, I980b). These experiments are summarized in Table VT, where the molecular species patterns for different lipid classes are shown. In temperature-shift experiments it has been found that A . variahilis rapidly alters its fatty acid composition as well as the positional distribution of such acids on individual glycerolipids. For example, for 10 h after a change in growth temperature from 38 ’C to 28 ‘C, the total amounts of lipids

LIP113 METABOLISM IN ALGAE

19

stayed constant but a desaturation of palmitate at the . ~ n - 2position of M G D G took place (Sato and Murata, 1980a). Molccular oxygen was required for the desaturation, which was prevented by chloraniphenicol or rifanipicin, suggesting that the specific A9-desaturase activity was induced by the downward shift in temperature (Sato and Murata, 1981). Slower decreases in the amounts of oleate and linoleate and commensurate increases in 3-linolenate which occur in M G D G and SQDG and PG were also prevented by protein synthesis o r R N A synthesis inhibitors (Sato and Murata. 1981). Conversely, sudden increases in growth temperature transiently increase de novo fatty acid synthesis but suppress desaturation of existing lipids in A . vuriuhilis (Sato and Murata, 1980a). The rapid changes in unsaturation levels of C , , acids only occurred in M G D G , in keeping with its role in palmitate desaturation (above). Slower changes in the unsaturation of C , fatty acids occurred in all major lipid classes (Murata, 1987). The changes which were found in the lipids of cyanobacterial membranes have been related to an adaptive response to prcvcnt damage caused by low temperatures. The results have been fully discussed (Murata. 1987: MuraLa and Nishida, 1987). I t appears that the plasma membrane (rather than the thylakoids) is particularly susceptible to low-temperature stress in both A nucysl is n iduluns and A nuhuenu vur iuhilis. Apart from temperature, a number of other environmental factors have been shown to alter lipid composition in cyanobacteria. These eKects are summarized in Table V11. Mention was made of the unusual heterocyst glycolipids a t the beginning of this section. These compounds have the structures shown in Fig. 8. The biosynthesis of these glycolipids was first studied by [I4C]acetate incorporation (Abreu-Grobois c t d . ,1977). I t was suggested that hydroxylation of the aliphatic chain at the C-3 and C-25 positions took place after the fatty alcohol was linked to the glycosides. Krespki and Walton ( 1 983) compared the formation of heterocyst glycolipids and glycerolipids during heterocyst formation. They concluded that biosynthesis of the hydrocarbon moieties of heterocyst glycolipids was regulated independently of fatty acid synthesis. In addition, they suggested that a n enzyme system for the hydroxylation of aliphatic hydrocarbon chains of the glycolipids was activated transiently during heterocyst formation. This process and heterocyst glycolipid synthesis are both increased by 7-azatryptophan (Krepski and Walton, 1983). Mohy-UdDhin el ul. (1982) suggested that the latter increased one or more steps of primary alkanol synthesis, making the (2-25 hydroxylation rate-limiting for the formation of the glycoside containing 1,3,-hexacosanetriol.

VI. STUDIES WITH HALOTOLERANT AND HALOPHILIC D U N A L I E L L A SPECIES Dunuliclla spp. possess some special features which make them attractive ex-

20

Environmental change

JOHN L. HARWOOD A N D A. LESLEY JONES

Organism

Effect

Reference

Nitrate increase ilnciej~s1i.rnidu1un.s .Spirul/nu pltrtc~I1.si.s Microc,j,stisuerugiiioscr 0.5cillur oriu ru hrscens

16:01 I 6 : I f 18:2t 18:31 N o change N o change

Piorreck ei nl. (1984) Piorreck P I a/. (1984) Piorreck ei ul. ( 1 984) Piorreck P I uI. ( 1984)

Increasing culture age

Agnienrlluni yuurlruplicuruni Anuh~rrnrrwriuhilis

16: 1. 18: It 1 8 : 2 , Olsonandingram 18:3J ( 1975) 18: l t 1 6 : O . 1 8 : 2 1 Gusevrru/.(1980)

Anaerobic growth

Apli~tio~lirc~c~ hulophj~ticu18 : 21 O.sc,iNtrtoriu linineticu No change

Oren ei a / . ( 1985)

Light presence

Various

No change

Kenyon el ul. ( 1972)

Light intensity

Anuc.j.sti.7 riidulnns

16:0, 1 8 : I f 1 6 : I J DohlerandDatz with increased light (1980)

Light quality

Anrrc~j~sti.~ nit1ulnn.s

GI ycerolipid changes

Temperature drop

Various

Chain length1 Unsaturationt See text Molecular species changes

Datz and Dohler (1981)

Fatty acid abbreviations as in Table I

perimental models. They grow rapidly under axenic conditions to yield populations of very homogeneous cells. Since they are without cell walls, they are easily disrupted and can therefore be separated into relatively pure subcellular fractions. Their lipid composition is rather similar to that of higher plants and is typical of green algae. Moreover, their ability to tolerate a wide range of temperatures and salinities (Brown and Borowitzka, 1979) allows the effects of these environmental stresses on metabolism to be studied. The lipids of two halotolerant species of Dunuliellu, ( D . purva and D.terriolectu) (Evons et ul., 1982a) and six halophilic species (D.viridis from the Dead Sea and various unidentified species from the Sinai) (Evans and Kates, 1984) have been examined. All these species were found to contain high proportions (40 mol %) of glycosylglycerides and low proportions (20 mol YO) of phosphoglycerides. The main glycolipids were MGDG, D G D G and SQDG. The main phospholipids were PG and PC. Analyses for the two halotolerant and two halophilic species are shown in Table VIII.

21

LIPID METABOLISM IN ALGAE

Glycosyl ester glycobpids

Glycosd~cglycolipi@

a-0-Glucopyranos yl 25-hydroxyhexacosa~te

3,2 5-Dihydroxyhexacosanyl-0-D-glycopyranoside

no

no

0- a n d

on

no ou

( 9 0 -1. )

0-D-Glucop yranosyl 25.27-dihydroxyoctacosaMte

Fig. 8.

OH

( 1 0 'I. )

YY

noon

on

3,25.27-Trihydroxyoctacosanyl-a-Dglycopyranoside

Structures of heterocyst glycolipids of cyanobacteria

TABLE VIII Lipid composit ion of h u b tolerant and haloph ilic Dun a I iella species Lipid

D. parva

Phosphatidylcholine Phosphatid ylethanolamine Phosphatidylinositol Phosphatid ylglycerol Phosphatidic acid Total phospholipid

9 n.d. 2 6 n.d 17

Monogalactosyldiacy lglycerol Digalactosyldiacylgl ycerol Sulphoquinovosyldiacylglycerol Other glycolipids Total glycolipids

21 II 7 I -

Diacylglycerol-0-(N,N,N-trimethyl)homoserine Non-esterified fatty acid Neutral lipids

D. tertiolecta

4 2 3

8 2 -

C,

D, ,

1 1 tr.

2 1 tr.

4 3 tr. n.d -

19

6

6

22 21

22 19

24

3

9

7 25

15 14 14 tr. tr. 55 53

40

10 tr. 53

15

8

13 15

7

14

15

21

Data expressed as mol YOand taken from Kates (1987) with permission n.d. = not detected.

22

J O H N L. H A R W O O D A N D A . LESLEY JONES

In general, halophilic species had lower levels of phospholipids and proportionally higher amounts of glycosylglycerides than halotolerant species. Moreover, PI, which was found in appreciable amounts in halotolerant species, was only found in trace amounts in the halophilic species. PE was not detected in D. parva. Significant amounts of neutral lipids, principally triacylglycerols and nonesterified fatty acids, were found in all species. These represented 15-25 mol YO and 7-14 niol ‘4, respectively, of the total lipid contents. Interestingly, diacylglycerol-O-4’-( N.N,N-trimethyl)-homoserine was identified as a major component (3 ~ 1 mol 4 Y O )in all species examined (Evans et al.. 1982b). As mentioned in Section 111, this zwitterionic non-phospholipid has been found in many algal species (Eichenberger, 1982; Sato and Furuya, 1985). including D. hrirckau~il(Fried Ct a/., 1982). I t is common also in lower plants (Sato and Furuya, 1984a,b) but has not been detected in any angiosperms or gymnosperms examined. The fatty acids of individual lipid fractions from all Dunalirlla species showed characteristics typical of other plant types, including angiosperms. Thus, palmitate was the major saturated fatty acid and this was enriched in SQDG of the glycolipids. The two galactosylglycerides were enriched in polyunsaturated fatty acids. MGDG was enriched in a-linoleic and hexadecatetraenoic acids. while DGDG contained high amounts of linoleic and x-linolenic acids. DGTS also contained a similar fatty acid content to DGDG. As in higher plants, PG contained high amounts of trans-A3hexadecenoate as well as appreciable amounts of palmitate, linoleate and alinolenate. D . .salina has been extensively studied at the subcellular level by Thompson’s group. Firstly, studies were made of phospholipid metabolism during growth at 30 C or 12 C or after temperature shifts. Generation times were found to correspond approximately to a Q,, of 2. with times of 20 h at 30 C and 80 h at 12 ‘C. Both cultures reached the same cell density but had rather different lipid and protein contents. In general, cells cultured at 12 C had a higher protein and acyl lipid content but a lower chlorophyll content than those grown at 30 C. Interestingly, the chlorophyll ujh ratio was 2.77 at 30 C but 4.09 at 12 C (Lynch and Thompson, 1982). The relative changes in acyl lipid and chlorophyll contents could be correlated with a proportional decrease in thylakoid membranes but an overall increase in cell volume at 12 C. When cells were shifted from 30°C to 12”C, no division occurred for about 96 h, after which division resumed, with a generation time of 80 h. The major particulate subcellular fractions were the chloroplast and microsomal. Whereas the chloroplast fraction was enriched at least four-fold in glycolipids compared to phospholipids, the microsomal fraction contained about twice as much phospholipid as glycolipid. Moreover, the relative proportion of cell phospholipid contained in chloroplasts was significantly reduced when cells were shifted to, or grown at, 12°C. This reflected the relat-

LIPID METABOLISM IN A L G A E

23

ive increase in microsomal menibrancs compared to thylakoids for cclls grown at lower temperatures (Lynch and Thompson, 1982). When the proportions of individual phospholipids of chloroplast or microsoma1 membranes were analysed, they were found to change little with growth temperature. For cells grown at either 30 C or 12 C, the major phospholipids of chloroplasts were PG and PC with smaller amounts of PE and PI. Microsomal menibranes contained PE and PC as the main phospholipids. In contrast, the relative proportions of glycolipids responded to temperature change. In particular, the relative content o f D G D G increased and that of M G D G decreased at 12 C. The ratio of M G D G to DGDG therefore changed from 3.4 in chloroplasts from 30 C cells to 2.1 for 12 C cells. Because poikilotherms need to maintain membrane fluidity at different growth temperatures, it was not surprising that phospholipid unsaturation was increased at 12 C for both chloroplast and microsomal membranes. In temperature-shift studies. the majority of these changes occurred after more than 60 h for chloroplast fatty acids. In the microsomal fraction, significant decreases in palmitate and increases in octadecatrienoate contents were seen within 12 h of temperature shift. Similarly, changes in the fatty acyl content of DGTS were also greater in the microsonial membranes. In contrast, the fatty acid patterns of the chloroplastic glycolipids changed little in response to growth temperature (Lynch and Thompson, 1982). The rather slow response of fatty acid unsaturation to shifts in growth temperature--especially for the chloroplast membranes-raised the obvious question as to how poikilotherms are able to withstand sudden changes in environmental conditions. Following observations with cyanobacteria (Section V), where an “emergency response” seemed to be the retailoring of individual molecular species (Sato and Murata, 198Oa,b), the phospholipids of D..sulinu membranes were examined in more detail. The individual phospholipids were isolated following thin-layer chromatography (TLC). a n d converted to diacylglycerols by digestion with phospholipase C; the diacylglycerols were separated by G L C of trimethylsilyl derivatives. Such procedures showed that there were significant changes in the molecular species of PE and PG. F o r PE there was a decrease in C,, species and co,ncomitant increases in C,, and C,, species. Changes associated with PG included the detection of a new molecular species, dioleoyl, not found at 30 C. Although there were some, limited, changes in fatty acid unsaturation detected during the first 12 h of low-temperature acclimation, it was concluded that the initial alterations in response to low temperatures involved discrete changes in certain molecular species. Such changes in molecular species composition would then augment the effects of acyl chain unsaturation in modifying membrane fluidity (Lynch and Thompson, 1984a). As mentioned above, changes in the fatty acyl composition of chloroplast phospholipids were much slower than for microsomal components. Thus only minor alterations in phospholipid acyl chain compositions were evident

24

JOHN L. HARWOOD A N D A. LESLEY JONES

after 36 h of shifting cells from 30 to 12 C. Between 36 h and 60 h, increases in the percentage of palmitate and a-linolenate were observed in PG. These alterations were accompanied by decreases in trans-A3-hexadecenoate and linoleate (Lynch and Thompson, 1984b). In contrast, the fatty acyl composi:ion of the other main chloroplast phospholipid, PC, did not alter very much over the 60-h period. Changes in the molecular species distribution for PC and PG were also seen after 60-h acclimation. The molecular species changes for PG correlated well with the overall fatty acyl changes. Thus, the 18 : 2/16 : I species was particularly reduced, in keeping with the decrease in both linoleate and rrans-A3hexadecenoate. Significant increases in molecular species containing palmitate and r-linolenate were seen-again in keeping with the fatty acid analysis (Lynch and Thompson. I984b). The change in molecular species of PG which occurred between 36 h and 60 h, following a shift in growth temperature, coincided with a large change in the threshold temperature of thermal desaturation of the photosynthetic apparatus. This was measured by chlorophyll fluorescence and, since lipid compositional changes other than those associated with PG were negligible during this period, suggested that a correlation existed between the molecular species of composition of PG and the thermal stability of the photosynthetic membrane. Taken together with the data on microsomal membrane compositional changes, the experiments suggested strongly that the initial steps in cellular acclimation to low temperatures involved molecular species retailoring. These changes then augmented the effects of increased acyl chain unsaturation as a means of restoring appropriate membrane properties (Lynch and Thompson, 1984~). Further studies on the subtle changes in acyl lipid molecular species used HPLC as the separation technique. Because of the poor absorbance of lipids in the UV. initial quantitation used the laborious procedure of effluent splitting and measurement by GLC of fatty acid methyl esters (Lynch and Thompson, 1983). However, the development of a flame ionization detector allowed more rapid quantitation and the procedure was applied to the analysis of D.sdina PG and galactosylglycerides (Smith et a/., 1985; Cho and Thompson, 1987). In Section IV, mention was made of the so-called prokaryotic and eukaryotic pathways for fatty acid and acyl lipid synthesis in eukaryotic organisms. The relationship between these two pathways in D.salznu was investigated in detail through radiolabelling with [I4C]palmitate, [I4C]oleate and [14C]laurateas precursors. Since only [I4C]laurate could be elongated in D. salina, palmitate gave rise to C,, acids only and oleate to C, , acids (Norman eta/., 1985). After a 2-min incubation with 4 pCi of [I-14C]palmitate, about 3% of the isotope was taken up per 5 x lo8 cells. This allowed experiments to be conducted with a 2-min labelling period followed by a chase period. During the total incubation a gradual movement of radioactivity was

LIPID METABOLISM IN ALGAE

25

seen from the microsomal membranes to the chloroplasts. This movement was associated with a decrease in phospholipid labelling and an increase in that of glycolipids. When the individual acyl groups were analysed, it was found that phospholipids only contained [I4C]palmitate. In contrast, glycolipids contained unsaturated C,, acids. After a 16-h chase, over 30% of the glycolipid radioactivity was accounted for by [14C]hexadecatetraenoate. Similarly, when [14C]oleatewas used in labelling studies, the radioactivity was incorporated initially into phospholipids of the microsomal membranes. After only a 20-min chase more than 50% of this microsomal phospholipid labelling was in the form of [*4C]linoleate,showing the presence of an active extra-chloroplastic A1 2-desaturase. By 16 h, chloroplast phospholipids contained 58% and 12% of their radioactivity in linoleate and sr-linolenate, respectively. In contrast, chloroplast glycolipids contained over 70% of their radioactivity as a-linolenate. These results confirmed that in D.salina, as in higher plants (Harwood, 1988), desaturation of oleate occurs mainly outside the chloroplasts, followed by transfer of the resultant linoleate back into plastids for its desaturation to a-linolenate in association with glycosylglycerides. When [I4C]lauratewas used as precursor, the acid entered the chloroplast quite rapidly, where it was used by the de n o w synthesizing enzymes and gave rise to radiolabelled C,, and C , , fatty acids. Moreover, in contrast to [ 14C]palmitate labelling, [‘4C]laurate incorporation resulted in the accumulation of appreciable [’4C]trans-A3-hexadecenoate. These studies were extended to a consideration of the molecular species of PG which were radiolabelled during temperature stress. When[14C]palmitate was used as precursor for a 2-min pulse, the specific radioactivity of PG was higher initially than that of any other microsomal phospholipid. The major molecular species of microsomal PG (80%) was 16 : 0/18 : 2, with about 45% of the 16 : O/ 16 : 0 species. Smaller amounts of 16 : O/ 14 : 2 species were also present (Lynch and Thompson, 1984a). In spite of the heavy concentration of 16 : 0 at the sn-l position, analysis of the radiolabelled PG by phospholipase A, digestion revealed that 30% of the [I4C]palmitate wgs present initially at the sn-2 position. In fact, immediately after labelling, the specific radioactivity of the palmitate at the sn-2 position was 10 times that at the sn- 1 position. Molecular species analysis by HPLC confirmed that [I4C]palmitate was preferentially incorporated into the 16 : 0/16 : 0 species. During the cold-chase period a changing pattern of incorporation of [L4C]palmitateinto either microsomal or chloroplast PG was seen. Thus, whereas microsomal PG always contained more radioactivity at the sn-l position, chloroplast PG initially contained radioactivity almost exclusively at the sn-2 position. With time, both positions of chloroplast PG became equally labelled. These results indicate the “prokaryotic” nature of chloroplast PG synthesis initially, and it is only later that molecular species of presumed microsomal origin appear in the plastid (Norman and Thompson,

26

J O H N L. HARWOOD A N D A. LESLEY JONES

I985a). I n fact, further analysis of the chloroplastic molecular species showed that 18: 2/16: 0 was labelled initially, followed only later by 16: Ojl8 : 2 species. When [I"C]laurate was used as precursor, the acid was rapidly taken up by chloroplasts, where it was used by fatty acid synthetase to produce [14C]palmitate and [14C]stearate, and the latter was desaturated to [14C]oleate.These products were rapidly exported to the endoplasmic reticulum, where PG was labelled more rapidly than other microsomal phospholipids. I n marked contrast, chloroplast PG contained no radiolabelled C , fatty acids. Immediately after the 2-min labelling period, this phospholipid contained large amounts of ['4C]laurate, but within 10 min of chase, [I"C]palmitate was the major radiolabelled moiety. In keeping with the proposal that 1 -acyl,2-palmitoyl-PG is the substrate for the A3-desaturase (Harwood and James, 1975), the decline in radioactive palmitate during the 20-60-min chase period was matched by an equivalent rise in the labelling of truns-A3-hexadecenoate. As mentioned above. the proportions of dilrerent cellular membranes in Dutitrlir//rr changes with low-temperature growth. There were also significant changes in the metabolism of chilled cells. Thus, for example. there was no delay in the labelling of the sn-l position of chloroplast PG from [lSC]palmitatein chilled cells. This was due to the increased contribution of "eukaryotic" (microsomal) metabolism at lower temperatures. Moreover, this was in keeping with the previous observations that the molecular species composition of microsomal PG responded more quickly to temperature stress than that of chloroplasts (Lynch and Thompson, 1984a.b). If niicrosomal phospholipids are retailored initially in response to temperature stress. then there should be appropriate enzymes present to remove and re-esterify the different acyl groups (Lynch and Thompson, 1984~).The first enzyme needed would be a phospholipase A and, indeed, such an enzyme has been reported in D..su/inu (Norman and Thompson, 1986). Microsomes, but not chloroplasts. contained a fatty acyl hydrolase with high activity towards endogenous or exogenous PG and PE. The enzyme had little activity towards other phospholipids or MGDG. Because no monoacyl products could be detected, it was not possible to analyse independently the activities of any specific enzymes, such as phospholipase A , or A,, or lysophospholipase which might be present. Lipolysis was most active in the presence of 10 mM C a 2 + , and was enhanced by calmodulin and inhibited by calmodulin antagonists, such as W-7 or 48/80. Most interestingly, the acyl hydrolase activity of 30 C-grown cells was low when measured in vitro at 12 C. However, when cells were chilled to 12'C, activity as measured at 12 C in vitro rapidly increased, thereby providing the mechanism for retailoring phospholipids during low-temperature acclimation. The low acyl hydrolase activity in chloroplasts from similarly treated cells emphasized the key role of micro-

27

LIPID METABOLISM IN ALGAE

18:1/16:0 MGDG

18:2/16:0 DGDG 18 1/16 1 MGDG

18 1/16 1 DGDG

18 3/16 0 DGDG

D' s

18 3/16 4 MGDG

>18

3/16 4DGDG

l i g . 9. Pathways for galactosylglyccridc synthesis in Diititrlidltr plasts. Redrawn from Cho and Thompson (1987) with permission.

.srr/inti

chloro-

soma1 metabolism in temperature adaptation (Norman and Thompson, 1986). Although the labelling of galactosylglycerides in D.siilinu has not been studied in as much detail as that of the phospholipids. a recent report describes labelling of molecular species from I4C-labelled fatty acids (Cho and Thompson, 1987), and a fatty acyl hydrolase preferentially attacking MGDG has been reported (Cho and Thompson, 1986). The results of the labelling studies are summarized in Fig. 9. They showed that, as expected (Harwood, 1988), the initial molecular species of MGDG labelled by &novo synthesis was the 18 : 1/16 : 0. This molecular species could then be further desaturated at both positions to eventually produce the highly unsaturated 18: 3/16:4 species. However, after the initial desaturation to 1 8 : 1/16: I , this species (like others) of MGDG was a substrate for galactosylation. The DGDG so produced was itself a substrate for continued desaturation. The 18 : 1/16 : 0 species of MGDG could be galactosylated but the DGDG so produced could only be desaturated at the sn-l position to yield a-linolenate. No further metabolism of palmitate at the sn-2 position took place (Cho and Thompson, 1987). These observations are particularly interesting because not only do they provide further evidence for the involvement of complex (galactosylglycerides) lipids as substrates for desaturations, but they also confirm that ( I ) lipid-linked acyl chains can be subject to a whole series of desaturations and ( 2 ) that several lipid types (in this case DGDG as well as MGDG) may serve as substrates for an individual desaturation. These topics are reviewed more fully in Harwood ( 1 988).

28

JOHN L. HARWOOD A N D A. LESLEY JONES

VII.

METABOLISM I N MARINE ALGAE A.

LABELLING CHARACTERISTICS

There have been relatively few studies on the lipid metabolism of marine macroalgae. There is now, however, a considerable body of work on their lipid and fatty acid compositions. Earlier work in this area has been summarized by Pohl and Zurheide (1979a). Most of the lipids which are found in marine algae occur in higher plants, although there are exceptions, and marked contrasts are seen in the lipid patterns of different algal divisions (Table IX). Marine algae have a characteristic pattern of polyunsaturated fatty acids which is quite distinct from that of higher plants (see Section Ill), and again reflects differences among the algal divisions (Pohl and Zurheide, 1979a). These observed differences in marine algal lipids and fatty acid content are presumably a reflection of differing metabolism, but there is very little detailed information available. The marine algae typically contain high proportions of polyunsaturated fatty acids (e.g. Jamieson and Reid, 1972; Pohl and Zurheide, 1979a). The brown and red algae contain arachidonic (20 : 4. w-6,9,12,15) and eicosapentaenoic (20 : 5 , w-3,6,9,12,15) acids as major fatty acids, with the brown algae tending to have more of the former and the red algae more of the latter. The green algae have only small amounts of C,, fatty acids, but do contain C,, and C , , fatty acids, which are more unsaturated than those of higher plants. Entrromorphu intrstinalis, a marine green macroalga, has among its major fatty acids a-linolenic acid ( 18 : 3, w-6,9,12), which is typical of higher plant photosynthetic tissue, and also octadecatetraenoic (18 : 4, w-3,6,9,12) and hexadecatetraenoic ( 1 6 : 4, w-3,6,9,12) acids (Jones and Harwood, 1987). Octadecatetraenoate is found in some higher plants, e.g. borage (Stymne rt ul., 1987). In this species, octadecatetraenoate is formed from cz-linolenate while esterified to MGDG (Griffiths et al., 1988). Labelling studies on the fatty acids of algae using [I4C]acetate show that the major fatty acids labelled are generally palmitate and oleate. Incorporation of radioactivity into palmitoleate, stearate and the more polyunsaturated C ,, fatty acids with long-chain C,,, C,, and occasionally C,, saturated fatty acids (Table X), is usually seen also. This indicates that the initial pathway of fatty acid synthesis is similar to that of higher plants, but that additional desaturase and elongase enzymes must be present for the production of the complete marine algal fatty acid pattern. The long-chain polyunsaturated fatty acids are themselves synthesized slowly, as indicated by time-course studies for up to 24 h with [I4C]acetate, when n o radiolabel accumulates in arachidonate or eicosapentaenoate (Jones, A. L. and Harwood, J. L., unpublished). A preliminary report for Porphyra yezoensis suggests a route for chain elongation and desaturation in this alga, but further studies are needed to confirm this (Kayama et al., 1986).

TABLE IX The lipid composition of marine algae representing different algal divisions Lipid

Phaeophyta

Rhodophyta

Chlorophyta

F. serratus

F. vesiculosus

Ascophyllum nodosum

Chondrus crispus

Polysiphonia lanosa

E. intestinalis

MGDG DGDG SQDG X

18.1 23.1 32.9 7.5

15.0 11.3 22.0 24.1

19.7 16.6 19.4 17.2

17.6 12.8 14.7 n.d.

17.6 24.6 11.9 n.d.

45.9 14.8 14.8 n.d.

PC PE PG PI DPG DGTS

4.3 5.7 2.5 2.1 4.2

4.2 6.2 2.2 2.9 5.4

3. I 9.8 1.5 2.5 3.1

31.6" 1.8 8.2

18.3" 1.5 5.0

-

-

-

4.9

5.0

7.6

15.0

1.8

2.1

1.8

2.7

NL

Rest

1.6

Data as means n = 3-7; X, unidentified glycolipid; n.d., none detected. Results expressed as YOtotal lipid "PC+ PSC

-

1.5 -

2.6

1.5

-

13.7

3.3

30

J O H N L. H A R W O O D A N D A. LESLEY J O N E S

TABLE X Rudioluhelling

(?f:firttj'acids f r o m

[ ' 4C]uce1ate in various marine algae

Fatty acid (YOtotal fatty acids) 1 4 : 0 16:0 16.1 18:O 1 8 : l 1 8 : 2 2 0 : 0 22:O Others Phaeophyta F. si~rrutiis 5 F. i~e.cicu1osu.c 3.4 A.vc~op/ivlluninorlosion 2.6

42.0 16.0 19.9

Rhodophyta C'honclrus c ~ i ~ p t i . s Polj~siphoniuItrrro.srr

I .5 6.5

5.7 40.9

Chlorophyta E. intc.stinu1i.s

1.7

9.8

13 I 17 1.8 12.1 41.1 tr 11.6 43.3

2 3.8 4.8

6 5.3 4.0

12.0 10.9

3.8 62.6 7.2 21.5

4.3

3.5 4.8

2.8

2.2 42.1

9.2

~

2.9

10 8.9 9.2

4 7.7 4.1

4.6

2.8

~

~

8.7

16.5"

" ~ 1 83: + IX.4: tr

= <0.5"%. Labclling X h in the light at 15 C. F. .serru/u.s at 20 C . Fatty acid abbreviations as for Table I . Data for F. .scrrLrfu.sfrom Smith a n d Harwood (1984a). Othcr d a t a from Jones. A . L. a n d Harwood. J . L. (unpublishcd).

The major lipids of most of the marine macroalgae that have been studied are the glycolipids (Table IX). In the fucoids, Fucus vesiculosus, F. serriitus and Ascophylluni nodosuni, they account for 70- 80% of the total acyl lipids (Smith and Harwood, 1984a; Jones and Harwood, 1987). Similarly high proportions are found in the red and green algae (Pettitt et d.,1988b; Jones and Harwood, 1987) as well as in cyanobacteria and some fresh-water green algae (Section 111). The leaf tissues of higher plants have comparable proportions of glycolipids (Harwood, 1980a), but higher plants generally have more MGDG (25-45%) and less SQDG (10%). All the marine algae so far examined have significantly more SQDG (Table IX). E. intestinalis has the glycolipid distribution most similar to that of higher plant leaf tissue, with 46% MGDG. It has been postulated that the high levels of glycolipids in algae indicate their location in membrane systems other than the chloroplast thylakoids (Smith et ul., 1982). This idea is partially supported by work on Polj,siphonia lunosa, which indicated that the chloroplast lipid content was similar to that of the whole tissue (Pettitt, T. P. and Harwood, J. L., unpublished results). In most of the algae studied, the glycolipids appear to be similar to those of higher plants. However, some unusual glycolipids have been detected. PhamQuang and Laur (1976a,b,c) reported unusual glycolipid structures in several fucoids, and other sugars (such as mannose and rhamnose) have been detected which may partly replace the galactose of MGDG and SQDG in the red algae Chondrus crispus and Polysiphonia lanosa (Pettitt and Harwood, 1986). Pham-Quang and Laur (1976b) found unusual sulpholipids in some

31

LIPID METABOLISM IN A L G A E

Ascoplij~llunitiodosuni

Lipid

"o/

I4C Lipids

F. wsicdosus

F. sewatus

"h I4C Lipids

YOI4C Lipids YO3 2 P Lipids

5.8 1.4 13.2 16.3

8. I 2.1 12.5 28.4

9.2" 4.P 9.0 19.2

1 .9 6.3 4.4 I .4 6.9

2.3 6.8 3.9 2.6 3.7

2.4 4.0

Neutral lipids

17.4

23. I

11.3

Rest

25.3

6.5

4.0

MGDG DGDG SQDG

X PC PE PG DPG PI

2.3

5.4 50.0 7.0 12.2 15.4

10.0

"MGDG includes DPG. *DGDG includes PG. Data as means. I I = 2 or 3 . Jones, A. L. and Harwood, J. L. (unpublished) and Smith P I cil. (1982)

fucoids, and Chondrus crispus and Polysiphoniu lunosu contained lipids other than SQDG which were detected by 35S-labelling. In both these red algae one of these sulpholipids was probably PSC (Pettitt et ul., 1988b), the sulphurcontaining analogue of PC first noted in the diatom N . ulhu (Anderson et ul., 1978a,b). The glycolipids of the brown algae F. serrutus, F. vesiculosus and Ascophyllum nodosum tend to be poorly labelled from [I4C]acetate in relation to their abundance (Table XI). However, SQDG is well labelled, particularly in Ascophyflum notlosum. This may be a reflection of the higher proportion of C , , and C ,, saturated and mono-unsaturated fatty acids in SQDG, because such acids are more rapidly labelled than the polyunsaturated C,, fatty acids which constitute a major proportion of the MCDG and DGDG acyl chains. MGDG has a higher proportion of label at all incubation times than DGDG, and this may partly reflect a possible role as substrate for the desaturation of linoleate to linolenate, by analogy with higher plants (Roughan e f ul., 1979; Wharfe and Harwood, 1978). However, any discussion of desaturationelongation reactions in these marine algae is complicated by the presence of a much greater variety of polyunsaturated fatty acids than occurs in higher plants. Another notable feature of lipid labelling in these algae is the high propor-

32

JOHN L. HARWOOD A N D A. LESLEY JONES

T A B L E XI1 Unsaturrctron indices of red and brown algal glycoliprdJ Lipid

F. vesiculosus Ascophyllum nodosum

Chondrus crispus

Polysiphoniu

Porphyrtr

lanasa

.13rzoensis

MGDG

3.5

3.4

4.6(1) 2.1 (2)

4.0(1) 2.4 (2)

4.8 ( I ) 2.3 (2)

DGDG

3.1

2.8

2.1

2.4

3.6

SQDG

1.5

0.8

3.4 ( I ) 1.9 (2)

I .4

2.5

Unsaturation index

( % ratty acid x no. double bonds)

= ~-

~~~

~

~~~~

I00

Where twc: bands were detected by TLC. the raster running band is designated ~ ~ ( ~ : o ~ data m i . sfrom Araki (I!ul. (1986).

( I ) . Porphyrci

tion of label found in lipid X (Table XI). This unknown lipid is clearly an important constituent of the fucoids, but its role in metabolism is difficult to assess, as it remains unidentified (Smith and Harwood, 1984a; Jones and Harwood, 1987). It is an acyl lipid with no net charge which stains positively with Dragendorf reagent, indicating the possible presence of a quarternary amino group. It does not contain phosphorus or sulphur. In Chondrus crispus the glycolipids are all poorly labelled from [I4C]acetate, but in Polysiphoniu lanosa the proportion of label in these lipids is much higher (Pettitt, T. R. and Harwood, J. L., unpublished). In E . intestinalis, SQDG is poorly labelled but MGDG and DGDG are fairly well labelled. As noted previously, the fatty acid and lipid pattern of E. intestinulis is different from that of the brown and red algae and, therefore, differences in lipid labelling are not unexpected (Jones and Harwood, 1987). In all these algae, as in higher plants, MGDG is the most unsaturated lipid (Smith and Harwood, 1984a; Jones and Harwood, 1987; Pettitt and Harwood, 1986). The relative unsaturation of the glycolipids of brown and red algae is shown in Table XII. Double bands occur on TLC for DGDG of F. vesiculosus and Ascophyllum nodosum (Jones and Harwood, 1987), for MGDG and SQDG of Chondrus crispus (Pettitt et al., 1988a; Jones and Harwood, 1987), and for MGDG of Porphyra yezoensis (Araki et d., 1986) and Polysiphoniu lanosa. The faster running band (band 1) has a higher unsaturation index in all cases (Table XII). Separation of double bands is caused by binding materials in commercial silica gel plates. The more saturated band is generally more highly labelled (Pettitt et al., 1988a). A similar range of phospholipids is found in marine algae to that of higher plants. All the eukaryotic marine algae so far examined have PG with trans-

LIPID METABOLISM IN ALGAE

33

A3-hexadecenoate, typical of higher plant chloroplasts (see Gounaris et al., 1986). As granal stacking is limited in the brown algae and does not occur in the red algae, this is further evidence that this is not the role of trans-A3hexadecenoate (e.g. Roughan, 1984). Caron et al. (1985) reported PG containing trans-A3-hexadecenoate to be preferentially associated with the lightharvesting complexes of F. serratus, but point out that its role may not be the same in algae as in higher plants. PE is the major phospholipid of the brown algae and PC of the red algae. PE and PC in the brown algae and PC in the red algae are highly unsaturated and tend to be only poorly labelled from [14C]acetate (Table XI). Arachidonate and eicosapentaenoate tend to be major components of these lipids (Section 111). The only detailed study of phospholipid metabolism in marine algae is that of Smith et al. (1982). [32P]Orthophosphate labelling in F. serratus showed phosphatidate to be labelled at short time intervals, with labelling decreasing as the incubation time increased, a result which would be expected if phosphatidate is an intermediate in phospholipid biosynthesis (Moore, 1982; Harwood, 1989). A concomitant rise in 32P-labellingin PI and PE was seen, although PC was poorly labelled at all time intervals. As PC was well labelled from [14C]acetate in this alga, such a result may reflect the role of PC as a substrate for desaturation of oleate to linoleate, as in higher plants (see Harwood, 1988). In E. intestinalis no PC was detected and only a small amount of PE. However, this alga contains DGTS, which was first reported in 0. danicu (Brown and Elovson, 1974). It has been found in various single-celled green algae (Eichenberger, 1982; Evans et al., 1982b), bryophytes and pteridophytes (Sato and Furuya, 1984b). As discussed in Section 111, various marine Chlorophyceae contain this lipid, including Ulva lucruca (Sato and Furuya, 1984b) and E. intestinalis (Jones and Harwood, 1987). In E intestinalis this lipid is a significant component (Table IX). It too is a Dragendorf-positive lipid with no net charge, but it does not have the same characteristics on TLC as the unknown lipid X of brown algae (Smith and Harwood, 1984a; Jones and Harwood, 1987). Eichenberger (1982) analysed several algal ‘species for the presence of DGTS and detected none in F. vesiculosus either. It has previously been noted that DGTS is often present in algae with little or no PC (Sato and Furuya, 1984a,b). In Chlamydomonas reinhardtii, which contains no PC, DGTS may be the substrate for the desaturation of oleate to linoleate, a role attributed to PC in higher plants (Schlapfer and Eichenberger, 1983; Section VIII). In D . salina, PC and DGTS are both present, and have similar fatty acid distributions. Metabolic studies using 14C-labelled fatty acid traces also indicate a close metabolic relationship between these lipids (Norman and Thompson, 1985b; Section VI). In E. intestinalis we have carried out labelling studies with [14C]acetate and found DGTS to be only poorly labelled compared with labelling of the glycolipids MGDG and DGDG and the phospholipid PG.

34

JOHN L. HARWOOD A N D A. LESLEY JONES

TABLE XI11 Percentage MGDG derived from prokaryotic (chloroplastic) or eukaryotic (cytoplasmic) pathways of lipid synthesis Prokaryotic or 16.[16

16-[18+20

Eukaryotic

Reference or

18+2~-r18+20 18+20-r16

Entcromorpha spp.

95

5

Ulva spp.

90

10

Rullkotter et al. (1975)

C. vulgaris

60

40

Roughan and Slack ( I 984)

Phaeodacrylum tricornutum

90

10

Arao et al. (1987)

Porphyra yezoensis

20

80

Araki et al. ( 1 987)

F. vesiculosus

10

90

Jones and Harwood (unpublished)

Heinz (1 977)

B. POSITIONAL DISTRIBUTION OF ALGAL FATTY ACIDS

In higher plants there are two pathways producing the diacylglycerol moieties for incorporation into glycolipids (e.g. Roughan and Slack, 1984; FrentZen, 1986; Joyard and Douce, 1987). The chloroplastic pathway produces lipids with a typically prokaryotic arrangement of fatty acids, i.e. with C , , fatty acids at the sn-2 position as in the cyanobacteria (Zepke et al., 1978). The PG of the photosynthetic membranes is of the prokaryotic type in all plants (Murata et al., 1982). The cytoplasmic pathway produces lipids with C,, fatty acids at the sn-2 position. Marine green algae generally show a prokaryotic fatty acid distribution in.their MGDG (Table XIII) (Rullkotter et al., 1975; Heinz, 1977). Phaeodactylis tricornutum (a marine diatom) also shows this typically prokaryotic MGDG (Arao et al., 1987). In F. vesiculosus, however, 10% of the C,, fatty acids are esterified to the sn-2 position of MGDG (Jones and Harwood, unpublished), and this is similar to published data for Chattonella antiqua (Sato et al., 1987), a raphidophyte and a member of the Chromophyta (organisms with chlorophylls a and c). More unusual is the situation in Porphyra yezoensis. In this alga only 20% of the MGDG appears to be derived from the prokaryotic pathway, yet the DGDG appears to be almost entirely chloroplastic in origin (Araki et al., 1987). On the basis of our current understanding of the synthesis of DGDG from MGDG in higher plants, it is difficult to see how this occurs (e.g. Joyard and Douce, 1987).

LIPID METABOLISM IN ALGAE

35

Sato et al. (1987) also noted positional specificity in the distribution of other fatty acids between the sn-1 and sn-2 positions in Chattonella antiqua. Eicosapentaenoate is enriched at the sn-1 position in MGDG, DGDG and SQDG, but at the sn-2 position in DGTS and PE. In Phueoductylis tricornutum, this acid was located at the sn-1 position in all the polar lipids except PC (Arao et al., 1987; Kawaguchi et al., 1987). In F. vesiculosus eicosapentaenoate is located (almost exlusively) at the sn-1 position in MGDG and DGDG, and mostly at the sn-1 position in SQDG (Fig. 10; Jones and Harwood, unpublished results), and preliminary results indicate that in PC and PE eicosapentaenoate occurs at both sn-1 and sn-2 positions. In F. vesiculosus MGDG and DGDG and Chattonella antiqua MGDG, octadecatetraenoate occurs at the sn-2 position, as it does in Borago (Stymne et al., 1987). These results from a range of algal species indicate some positional specificity in the transacylation (and, possibly, elongation) reactions for fatty acyl chains, and this specificity differs in both nature and extent in different algae. Generally, however, it appears that in the galactolipids of chromophytes, eicosapentaenoate is esterified to the sn-1 position (Fig. 10). Although C , , acids are not common membrane components of most terrestrial plants, they have been detected at the sn-2 position in some species (Auling et al., 1971).

C. EFFECTS OF THE ENVIRONMENT ON ALGAL LIPID METABOLISM

1. Light Light has a marked effect on the lipid composition of photosynthetic tissues in higher plants, synthesis of the typical chloroplast lipids MGDG, DGDG, SQDG and PG being stimulated in the light, as is the desaturation of their acyl chains (see Harwood, 1983). In Chondrus crispus the total amount of [' 4C]acetate incorporated in the light was higher than in the dark, and a marked increase was noted in PG labelling (Table XIV); this also occurs in Polysiphonia lanosa (Pettitt and Harwood, unpublished results). However, in F. serratus labelling of PG from [14C]acetatedid not increase significantly in the light (Table XIV), although a small but significant increase in PG labelling from [32P]orthophosphate did occur (Smith et ul., 1982). In Chondrus crispus, Polysiphonia lanosa (Pettitt, T. R. and Harwood, J. L., unpublished) and Bryopis maxima (a green marine alga) (Ohnishi and Yamada, 1977), light increased the proportion of oleate and linoleate labelled from [14C]acetate, with decreases in the amount of saturated fatty acids (Table XV). Algal metabolism in this respect appears similar to that of higher plants. The importance of the polyunsaturated C,, fatty acids is difficult to assess as they are labelled only slowly from [14C]acetate. This makes it difficult to study the effect of altered environmental parameters on these important fatty acids in vitro, although some conclusions can be drawn from a

36

JOHN L. HARWOOD AND A. LESLEY JONES

F. vesiculosus MGOG

8%~(~,

18: 18:4 2 65% 18:3

7%

OGDG

16%

1

18:4 5S0/

1 8 : 3 14%

18:2 12%

(3)

(2)

? i vezoensis MGDG

DGDG

-20:5 86% 16:O 9%

18:1 8% 18:2 5%

16:O 76% 18:l 9% 18:2 9%

(2I

-Gal.Gal

Fig. 10. Positional distribution of fatty acids in the galactosylglycerides of two marine algae. See text for details.

study of endogenous fatty acid content when algae are harvested under different environmental conditions. No results have so far been reported of the effect of light on the synthesis and occurrence of C,, fatty acids in marine algae. 2. Temperature Temperature is known to affect the lipid composition of many organisms, and these effects are thought to be a response of the organism to maintain fluidity in, and hence function of, membranes. The alterations that occur in

37

LIPID METABOLISM IN ALGAE

TABLE XIV Effect of light on radiolabelling from [32P]orthophosphateor [I4C]acetatein the acyl lipids of F. serratus and Chondrus crispus respectively

F.serratus'

Lipid

Dark

Chondrus crispusb Light

MGDG DGDG SQDG 54.3 f 5.9 10.3 f 1.0 4.9 f 1.9 9.8 f 0.6 1.4 f 0.4 19.3 f 2.9

PE PG PC DPG PA PI

52.1 f 8.6 11.6 f 0.8' 19.3 f 2.9 10.8 f 2.4 1.5 f 0.3 18.9 f 3.3

Dark

Light

10.3 f 0.2 1.9 f 0.4 9.3 f 0.6

14.3 f 2.6' 6.9 f 0.6 13.0 f 5.0

5.4 f 2.0 27.0 f 1.1

18.5 f 1.7' 17.6 f 2.9'

"Data from Smith er at. (1982). bData from Pettitt and Harwood (1987). 'P<0.05 Labelling in F.serratus was with [32P]orthophosphate and in Chondrus crispus with (I4C]acetate. Results are % of total acyl lipid labelled.

TABLE XV Effect of light on the distribution of radioactivity from [I4C]acetateamongst acyl chains in F. serratus and Chondrus crispus Distribution of label (YO14C-labelledfatty acids) 14:O

16:O

F. serratus' Dark 3.4 f 0.5 47.7 f 7.8 Light 3.2 f 0.4 31.5 f 5.4' Chondrus crispusb 6 f l Dark 1f 1 Light

31fl 19 f 2

16:l

-

2 f l 3f2

18:O

18: 1

18:2

Others

12.9 f 2.4 29.6 f 6.3 0.9 f 0.7 5.5 f 1.4 9.9 f 0.5 42.6 f 6.0' 9.4 f 1.6' 3.5 f 1.4 7&3 tr'

40f6 64f6'

3ftr IOfT

I l f l 3 f 5

'Data from Smith and Hanvood (1984b). bData from Pettitt and Hanvood (1987).

'P<0.05

Incubation for F. serratus was carried out for 7 h at 20°C. and for Chondrus crispus for 24 h at 15°C. Fatty acid abbreviations as for Table I.

38

JOHN L. HARWOOD A N D A. LESLEY JONES

plant membranes in response to decreased temperatures lower the phase transition temperature of the membrane lipids, and these effects have been best studied in the single-celled marine green alga D . salina (Section VI). Major strategies which maintain membrane fluidity despite lowered temperature are a reduction in fatty acid chain length, an increase in unsaturation and changes in positional distribution of acids. These changes have been seen in higher plants (Harwood, 1983) and Tables XVI and XVII show that they also occur in some marine algae. Some, but by no means all, higher plants also alter the levels of their complex acyl lipids (Clarkson er al., 1980), though this may also reflect a change in the subcellular morphology of responsive cells (see Harwood, 1989). The relatively constant endogenous fatty acid pattern of Ascophyllum nodosum in winter and summer has been noted before (Jamieson and Reid, 1972). However, many other algae do show increased unsaturation of their fatty acids in winter-the saturation indices of F. vesiculosus, Polysiphonia lanosa and Chondrus crispus are higher in February than in June (Table XVI). Pohl and Zurheide (1979b) reported increased unsaturation in F. vesiculosus and Phycodrys sinuosa from the Baltic Sea in the winter. Changes in unsaturation indices in F. vesiculosus follow very closely changes in sea-water temperature (Pohl and Zurheide, 1979b). In Polysiphonia lanosa the level of eicosapentaenoate-the most unsaturated fatty acid in this alga-drops significantly in the summer (Table XVI). In both Ascophyllum nodosum and Polysiphonia lanosa, labelling from [I4C]acetate shows increased unsaturation of fatty acids at 5°C compared with 15°C. In particular, labelling of the long-chain saturated fatty acids 20 : 0 and 22 : 0 is lower at 5"C, indicating less elongation of saturated fatty acids at lower temperatures. In Chondrus crispus there is increased labelling of C I 4 + C l 6fatty acids at 15°C and decreased labelling of C,, fatty acids, although a higher proportion of unsaturated fatty acids are labelled at 15°C (Table XVII). Another seasonal alteration in lipid metabolism is the distribution of label from [14C]acetate amongst the neutral lipids from algae collected in summer compared with those collected in winter. F. vesiculosus from the Baltic Sea was reported to have reduced triacylglycerol levels in winter (Pohl and Zurheide, 19796) and labelling patterns in F. serratus also change in a similar way. F. serratus collected in summer accumulates [14C]acetate into triacylglycerol, whereas in the winter, label was incorporated into unesterified fatty acids. This may, therefore, be related to an accumulation of triacylglycerol as a storage product in the summer with subsequent breakdown in the winter. In Chondrus crispus, increased labelling of SQDG and DGDG was seen at higher temperatures, and it has been suggested that a similar mechanism to that seen in wheat is in operation (Pettitt, T. R., Jones, A. L. and Harwood, J. L., unpublished). In wheat, modification of SQDG fatty acids occurs during temperature acclimation (Vigh et al., 1985). However, there is no

TABLE XVI Eflect of season on the fatty acid composition of red and brown algae Alga

Ascophyllum nodosum F. vesiculosus

Chondrus crispus Polysiphonia Ianosa

Fatty acid (% total fatty acid) 16:O

16:l

18:O

18.1

Feb. June

14

2 2

tr.

28 27

9 11

6

15

Feb. June

16 21

1

tr.

11

10

10

2

1

25

10

7

Feb. June

24 34

5 6

I

12 9

2

2

1

1 1

Feb. June

29 32

8 8

12 1

3

-

~

Data as means n = 2.3; tr. = <0.5%. Fatty acid abbreviations as for Table I. Jones, A. L. and Harwood, J. L. (unpublished)

1

tr.

1

18:2 18:3

5

18:4 20:4 20:5 Others

5

4

5 4

16 18

9 8

12 9

1.95 1.98

9 4

15 15

16 8

11 6

2.38 1.84

4

21 18

29 22

5 tr.

2.53 2.18

6 6

38 26

4 5

2.40 1.95

-

2

Saturation index

-

1

40

JOHN L. HARWOOD A N D A. LESLEY JONES

TABLE XVII Effect of temperature on labelling of fatty acids from [14C]acetate

Alga

Distribution of label (YO14C-labelledfatty acids)

Temperature (-C)

14:O 16:O 16:l 18:O 18:l 18:2 18:3 20:O 22:O Others

Ascophyllum nodosum

5 15

2 14 4 2 4

-

1 1 59 1 1 0 3 7

10

F. vesiculosus

5 15

3 13 4 1 8

tr 9 75 4 1 2 4 0

tr 7

Chondrus crispus Polysiphonia lanosa

5 15 5 15

1 2 8 37

10

3 8

23 36

-

8 t r tr 1

tr

tr

4

4

-

-

5

5

tr 4

-

3

-

2 tr

6 5

12 11

5 3 - - - - - 34 - - -

15 11

3 10

36 29

7

-

tr

-

2 4

4 9

1

2

Labelling for 24 h in the light: tr = <0.5%. Results from Jones, A. L. and Harwood. J. L. (unpublished).

indication in any alga so far studied of the alteration in ratio of PE to PC seen in frost-resistant rye (Clarkson et al., 1980). There are several possible molecular mechanisms for altering membrane fluidity in plants (see Harwood, 1989), most of which may apply to marine algae. The details of these mechanisms are generally unclear, although there are suggestions, for example, that desaturation rates may be linked to oxygen concentrations which are higher at low temperatures (Rebeille et al., 1980). The response of marine algal acyl lipids to changes in temperature is particularly complex in view of the relatively large range of their polyunsaturated fatty acids.

3. Heavy Metals The heavy metal concentrations to which marine algae are exposed vary with the consumption of the underlying rock and with the amount of pollution. The effects of industrial pollution may raise levels of heavy metals in sea water many-fold, especially for transient periods. The marine algae cannot prevent the uptake of metals, and accumulate them, often to 1 0 0 ~ 1 0 , 0 0 0 fold the concentration in sea water (Bryan and Hummerstone, 1973; Bryan, 1980). The metals are probably sequestered in cell walls or physodes of brown algae (Lignell et a f . ,1982; Smith et al., 1986), thus reducing potential toxicity. However, heavy metal exposure has been found to affect lipid metabolism, and a selection of green, red and brown algae have been studied. In E. intestinalis and Chondrus crispus, although Cu2' and Cd2+ are taken up by the algae, no effect on lipid metabolism was seen using either an acute or chronic incubation with the metals. The fatty acid labelling from

41

LIPID METABOLISM IN ALGAE T A B L E XVIII

EHect of Cu2+ on the ratio of counts found in the aqueous and organic phases of'a Garbus extraction

cu*

Alga

F. serratus

F. vesiculosus

+

( p g 1- 1 )

Ratio d.p.m. organic/aqueous

+ 0.6

0 30 300

4.4 f 1.7 4.0 f 0.2"

0 1000

3.5 f 1 . 1 7.1 f 1.2"

2.6

"Significantlydifferent ( P i 0 . l ) Results are means f S.D. (n = 3). The extraction method is described in Smith and Harwood (1984) and results are taken from that reference and Jones, A. L. and Hanvood, J. L. (unpublished).

[14C]acetatewas unaffected, as was the labelling of complex lipids (Jones and Harwood, unpublished). The best-studied marine alga with regard to the effects of heavy metals on lipid metabolism is F. serratus. Cd2+,Pb2 and ZnZ caused a decrease in the incorporation of [14C]acetateinto complex lipids, but few changes in the distribution of label amongst lipid classes (Smith and Harwood, 1984b). In this study the most notable change was that seen in the ratio of radioactivity between the organic and aqueous phases of a high-saltxhloroform-mefhanol-water (Garbus) extraction. Pb2+,Cd2+,Zn2+ and Cu2 all increased the ratio of counts in the organic phase of the extraction, but this was most marked for Cu2+(Smith et al., 1984, 1985). In vitro results for F. vesiculosus and F. serratus (Table XVIII)show this quite markedly. Further work has shown that lipid metabolism in F. serratus is more susceptible to Cuz than that of Ascophyllum nodosum or F. vesiculosus (Jones and Harwood, 1989, unpublished). However, the pattern of fatty acid labelling from [14C]acetate after incubation with Cu2+ in these brown algae is altered in a rather similar fashion (Smith et al., 1984; Jones and Harwood, 1988). Generally, labelled oleate levels are raised and palmitate levels lowered (Table XIX).Similar differences in endogenous fatty acids were seen in algae collected from sites heavily polluted with Cuz+ (Smith et al., 1985). If the pathways of fatty acid synthesis are similar to those of higher plants then it is possible that the activity of the acyl-ACP and/or acyl-CoA transacylases is being affected by Cu2+and other metals. These enzymes transfer acyl chains from thioesters into complex lipids. Palmitoyl-ACP is the initial product of the fatty acid synthetase enzyme system, and the condensing enzyme which adds the C, unit to give 18 : 0 is specific for this reaction (Shimakata and Stumpf, 1982). The desaturation of both palmitoyl- and stearoyl-ACP is carried out by a A9-desaturase. Thus, inhibition of palmitoyl-ACP acyl transfer would allow a higher flux of radioactivity through to oleate, while at +

+

+

+

42

JOHN L. HARWOOD A N D A. LESLEY JONES

TABLE XIX Effect ofCu2 on the incorporation of [I4C]acetateinto fatty acids +

Alga

YORadiolabelled fatty acid

Treatment

14:O 16:O 16:l 18:O 18:l 18:2Others F. serratus

Control 300pgCu2+ I - ' ( 1 hour)

7.5 74.2 1.5 4.3" 58.6" 3.1"

A scophyllum nodosum

Control 30pgCu2+ I - ' (8 days)

2.5 tr.'

21.1 17.1

F. vesiculosus

Control 120pgCu2+I - '

4.0 3.4

28.7 26.7

-

-

1.6 7.2 7.8 0.2 2.7" 15.6" 10.9" 4.8 12.8 62.0 1.6 6.0b 71.6" 3.7

-

0.9

15.6 28.0 1.6 22.0 12.7 34.1b 2.3 20.8

" P <0.0I 'P < 0.05 Fatty acid abbreviations as for Table 1. Data for F. serratus is from Smith el a/. (1984) and for the other algae from Jones, A. L. and Harwood. J . L. (unpublished).

the same time reducing palmitate labelling. At present, there is no experimental evidence to support such a hypothesis, but we are currently evaluating this possible mechanism.

VIII. LIPID METABOLISM IN OTHER ALGAL TYPES Although D . salina and the cyanobacteria are probably the best studied algae, work with some other algae, notably species of Chlorella, merits description here. Important work on the features of fatty acid desaturation was carried on C . vulgaris. The alga failed to desaturate added palmitate or stearate except when denied any carbon source. This was demonstrated by feeding [I4C]acetate under anaerobic conditions. Labelled palmitate and stearate accumulated but there was no desaturation under anaerobic conditions. However, on changing to aerobic conditions, [14C]stearate was converted rapidly to [ 4C]oleate, demonstrating the aerobic nature of the A9-desaturase (Harris et al., 1967). The substrate specificity of the desaturase system forming oleate was investigated with a series of radiolabelled acids from myristate (14 : 0) to nonadecanoate (19 :0) (Howling et al., 1968). Each was desaturated to the corresponding A9-monoenoate, but, in addition, myristate, pentadecanoate and palmitate yielded the A7-monoenoates. These results were interpreted as possibly indicating the presence of a A7-desaturase in addition to the main A9-desaturase, and, in addition, to show that the enzymes held

43

LIPID METABOLISM IN ALGAE

Substrate

Product

I

I

D-C-H

I I I H-C-D

DC _____)

D-C-H

I H-C-D

,I

H-C-D D-C-H

D-C-H H-C-D

I I I I

I I

,

-

II I I

DC

H

i

HC

I I HC I1 DC I I il HC I

(A)

(6)

(C)

DC

(D)

Fig. 11. Principle of experiment to demonstrate the reaction mechanism for stearate desaturation in Chlorella vulgaris. No isotope effect: twice as many monodeuterated products [(C) + (D)] as dideuteyated (A). Isotope effect at one position: equal numbers of mono- and dideuterated products. Isotope effect at both positions: product (A) formed preferentially. See Morris (1970) for details.

the substrate bound through the carboxyl group, probably as a thiol ester. The desaturation is highly stereospecific. Morris et al. (1967) incubated C . vulgaris with [erythro-9,10-*H,]stearate, [threo-9,1O-ZH,]stearate, [ ~ - 9 3H]stearate and [~-9-~H]stearate. Analysis of the oleate produced demonstrated that the desaturation involved the loss of the A9 hydrogen atom and of a pair of hydrogen atoms of cis relative configuration. Moreover, because there was an isotope effect at both positions, a stepwise reaction mechanism seemed unlikely and it was concluded that desaturation involves the simultaneous concerted removal of hydrogens (Morris, 1970; Fig. 11). Harris et al. (1965) showed that photosynthetically grown cells of C. vulgaris rapidly formed linoleate and a-linolenate by an aerobic process. Exogenous [1-l4C]stearate was converted to [l-14C]oleate and then [ l 14C]linoleate,showing the sequential nature of the desaturation pathway at the C,, level. Cell-free homogenates from such cells retained the ability to desaturate [l-14C]oleatein the presence of oxygen and NADH or NADPH (Harris and James, 1965). This activity was lost when the homogenate was separated into particulate and supernatant fractions. However, the particu-

44

JOHN L. HARWOOD A N D A. LESLEY JONES

late fraction regained activity if the substrate was added as [I-14C]oleoylCoA. Labelling experiments with C. vulgaris showed that PC became very highly labelled with regard to linoleate (Harris et al., 1967). This led to the suggestion that PC could be involved in oleate desaturation. In addition, further experiments suggested that other complex lipids could be involved in the different fatty acyl desaturations (Nichols et al., 1967). These were the first suggestions of a mechanism for desaturation involving non-thioester substrates, now accepted for, at least, the major pathways of polyenoate formation (Harwood, 1988). Direct involvement of PC in oleate desaturation was shown for Chlorella particulate fractions by Gurr et al. (1969). The chain length specificity of desaturases in C. vulgaris has been studied by Howling et al. (1968). They found that each of the A9-monoenates formed by the first desaturation could be desaturated further to form A9,12-dienoates (with the exception of A-tetradecenoate). Oleate was, however, the most active substrate. Further experiments were carried out with 8-heptadecenoate, 9-octadecenoate and 1 0-nonadecenoate, which yielded, respectively, A8,11-18: 2, A9,12-18: 2 and A10,13-18: 2 (where 18 : 2 stands for octadecadienoate). If the monoenoates were incorporated into a complex lipid before desaturation, then the concept of a desaturase having a specificity relating to the methyl end of the acyl chain is logical. Thus, it was concluded that C. vulgaris might possess two desaturases which were responsible for dienoic fatty acid synthesis. The first was a A12 desaturase which accepted A9-monoenoates, while a second 6-desaturase used 9-monoenates. Oleate would be a substrate for both enzymes. The stereochemistry of oleate and linoleate desaturation was demonstrated to be identical to that for stearate desaturation (Morris et al., 1967), i.e. cis elimination of hydrogen from the 12,13 or 15,16 positions involving the vic-D atoms took place. The presence of a very unusual fatty acid, trans-A3-hexadecenoate, exclusively located at the sn-2 position of leaf PG (Harwood, 1980a), was mentioned in Section 111. Similarly, C. vulgaris cells grown photosynthetically in the light accumulate the acid in this position exclusively. When organic nutrient is available, the acid is almost completely absent from cells, whether grown in the light or dark (Nichols, 1965). The biosynthesis of trans-A3hexadecenoate was investigated, and palmitate established as the direct precursor (Nichols et al., 1965). Desaturation was reduced in the absence of exogenous oxygen, indicating either a substrate requirement for the reaction or the need for oxygen in the supply of enzymes or cofactors involved. When [14C]trans-A3-hexadecenoate was added to C. vulgaris cells it was acylated to all lipids, showing that the specific location of the acid in PG in vivo was not due to a specific acyl transferase. The experiments showed that the most likely substrate for the desaturase was another complex lipid (I-acyl,2palmitoyl-phosphatidylglycerol),and this accounted for the specific location of the trans-A3-hexadecenoate product (Bartels et al., 1967). In addition, a

LIPID METABOLISM IN ALGAE

45

reductase system was found in Chlorella which could convert the transhexadecenoate to palmitate; such a system has been suggested to be involved in the function of trans-A3-hexadecenoate in thylakoid membranes (Harwood and James, 1975; Gounaris et al., 1986). Several workers have carried out general metabolic studies with green algae. Frequently, 14C0, and [I4C]acetate have been used. These have the advantage that radioactivity can be incorporated into all fatty acids (acyl groups) and, hence, into all classes of acyl lipids. However, the former, in particular, has the disadvantage that other parts of the lipid molecule are also well labelled (e.g. glycerol, sugars), leading to problems in interpretation. For this reason, [I4C]acetate is often a preferable precursor (Hitchock and Nichols, 1971). Optimal conditions for the incorporation of label from [I4C]acetate with C. pyrenoidosa have been worked out (Yung and Mudd, 1966). Using the same alga and 14C0,, Ferrari and Benson (1961) had earlier established the high metabolic activity of PG and MGDG during steadystate photsynthesis. Similar studies using [I4C]acetate and C. vulgaris showed that the rate of labelling of acyl groups of individual lipids was in the order:

PG > MGDG >PC > SQDG > PI > DGDG > PI This showed again, as with C. pyrenoidosa, that PG and MGDG were very rapidly labelled (Nichols et al., 1967). The rapid labelling of PG was also seen with [3ZP]glycerophosphatelabelling (Sastry and Kates, 1965). In a comparative study on lipid metabolism in C. vulgaris and two cyanobacteria, Nichols (1968) noted that the fatty acids of DGDG and SQDG were labelled much better in the blue-green algae. However, in all three organisms, MGDG was the best labelled of the glycosylglycerides. An important additional result from the general studies of lipid labelling with C. vulgaris was the demonstration that major changes in the fatty acid composition of individual lipids could take place after their de novo synthesis (Nichols et al., 1967; Nichols, 1968; Nichols and Moorhouse, 1969; Gurr et al., 1969; Safford and Nichols, 1970). This in turn led to the idea of a dynamic movement of acyl moieties between lipids and, more especially, to the concept that complex lipids can act as substrates for desaturation. These ideas have now been extended to all types of plants and were discussed briefly in Section IV. Fuller reviews of these aspects have been made recently (Stumpf and Conn, 1987; Harwood, 1988,1989). Chlamydomonas reinhardtii has been used as a useful experimental organism by a number of laboratories. Janero and Barrnett (1981a,b) reported on the detailed lipid composition of strain 137'. However, their results differed somewhat from the recently analysed arg-2 mt + strain (Eichenberger et al., 1986). The latter workers also noted the very similar lipid composition of a chlorophyll b-deficient mutant. Several workers have studied biogenesis of photosynthetic membranes. Beck and Levine (1977) used cultures which had

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been synchronized by a 12-h light/l2-h dark regime. They then followed incorporation of radioactivity into lipids using 35SO:-, 32PO:- and H14CO; as precursors. They concluded that while lipid synthesis occurred predominantly during the light part of the cycle, different (chloroplast) lipids were synthesized at different times. For example, PG was synthesized between 3 h and 4 h in the light, but SQDG was labelled between 7 h and 9 h. Galactolipid synthesis appeared to reach maximal rates at two times-immediately after the lights were switched on and after 7 h. All the lipids (and chlorophyll) were made and inserted into chloroplast membranes before any major increases in photosynthetic capacity were seen. The sequential nature of lipid insertion during membrane biogenesis was notable. These results were extended somewhat by Janero and Barrnett (1982), who looked at cell-cycle variations in the synthesis of PE and PC in nonphotosynthetic membranes. Peak incorporation of radioactivity from [14C]acetate was found around 7 h in the light. Thus, synthesis of thylakoid and non-thylakoid lipids in Chlamydomonas reinhardtii is confined essentially to the light period and occurs in mid-to-late GI. De novo synthesis of acyl lipids relies on the successive acylation of glycerol 3-phosphate to form the key intermediate phosphatidate. The two acylations concerned have been studied in Chlamydomonas reinhardtii (Jelsema et al., 1982). Both enzymes were very much increased upon light induction, the lysophosphatidate acyltransferase particularly so. The peak activities of the enzymes preceded thylakoid membrane biogenesis during the cell cycle. The enzymes were localized by cytochemical techniques, and activity was concluded to be associated with the chloroplast envelope (and in the pyrenoid tubules of the chloroplast and the Golgi apparatus and associated vesicles (Michaels et al., 1983)). The results are in keeping with a role for acyltransferases in chloroplast biogenesis as discussed for plants in general (Joyard and Douce, 1987; Hanvood, 1989). Mention has already been made of the involvement of various complex lipids in fatty acid desaturation. As described in Section IV, PC is thought to be the major substrate for oleate‘desaturation in plants (Harwood, 1988), including C . vulgaris (Gurr et al., 1969). However, in Chlamydomonas reinhardtii, PC is either absent (Eichenberger et al., 1986) or is present in very small amounts in non-thylakoid membranes (Janero and Barrnett, 198 1b). When labelling studies were made with [1-14C]oleate, DGTS was very rapidly labelled (Schlapfer and Eichenberger, 1983). Within 3 h about 80% of the labelled oleate incorporated into DGTS was desaturated to linoleate and linolenate. At the same time, label present in the 16 : 0/18 : 1 molecular species moved into 16 : 0/18 : 2 and 16 : 0/18 : 3 species. These data implied that DGTS acted as a substrate for the desaturation of oleate and linoleate. As further evidence for this role, radiolabelled di- 18 : 1-DGTS was used. The labelled lipid was di-([l-14C]oleoyl)-glyceryl-(N,”-tri-[3H]methyl)homoserine. Appreciable quantities of the intact lipid were taken up by the

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alga and, in part, its oleoyl moieties were desaturated as shown by the successive appearance of 18 : 1/ 18 : 2 and 18 : 1 / 18 : 3 molecular species. Interestingly, in relation to the possible role of DGTS in fatty acid desaturation, this lipid does not appear to be confined to one subcellular compartment. In Chlamydomonas, 15% (Mendiola-Morgenthaler er al., 1985) or 40% (Janero and Barrnett, 1982) of total DGTS is present in the thylakoids. In Dunaliella, 90% was located in the thylakoids (Norman and Thompson, 1985b). A careful subcellular fraction of Acetabularia mediterranea showed that the bulk of DGTS was found in microsomal fractions with a similar distribution to NADH
IX. CONCLUSIONS It should be clear from the foregoing sections that our knowledge of lipids, and especially their metabolism in algae, is poor. Only a few organisms have been studied in any detail, and in most algae which have been examined unknown lipids still remain t o be identified. Considering the tremendous variety of different algae, it will not be surprising to uncover many novel pathways for lipid synthesis in the future. Conceivably some of these metabolic differences may have important applications in other areas. Undoubtedly, the biotechnological exploitation of algae will become more prevalent in the next decade. However, it seems likely to us that, as in the past, the most

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significant discoveries will be made by scientists, inspired by a sense of curiosity, looking “where the light shines brightest”.

ACKNOWLEDGEMENT Work on algae in the authors’ laboratory has been supported financially by the SERC and the NERC, for which we are very grateful.

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Smith, K. L., Hann, A. C. and Harwood, J. L. (1986). Physiol. Plant 66,692-698. Smith, L. A., Norman, H. A., Cho, S. H. and Thompson, G. A. (1985b). J. Chromatogr. 346,291-299. Stapleton, S. R. and Jaworski, J. G. (1984a). Biochim. Biophys. Acta 794,24&248. Stapleton, S. R. and Jaworski, J. G . (1984b). Biochim. Biophys. Acta794,249-255. Stumpf, P. K. and Conn, E. E. (eds) (1980). “The Biochemistry of Plants”, Vol. 4. Academic Press, New York. Stumpf, P. K. and Conn. E. E. (1987). “The Biochemistry of Plants”, Vol. 9. Academic Press, New York. Stymne, S.,Griffiths, G. and Stobart, K. (1987). In “The Metabolism, Structure and Function of Plant Lipids” (P. K. Stumpf, J. B. Mudd and W. D. Nes, eds), pp. 405-412. Plenum Press, New York. Tornabene, T. G, Holzer, G., Lien, S. and Burris, N. (1983). Enzyme Microb. Technol. 5,435-440. Vigh, L., Horvath, I., van Hassell, P. R. and Kuiper, P. J. C. (1985). Plant Physiol. 79, 756759. Walker, K. A. and Harwood, J. L. (1986). Biochem. J. 237,4146. Wharfe, J. and Harwood, J. L. (1978). Biochem. J. 174, 163-169. Yung, K. H. and Mudd, J. B. (1966). Plant Physiol. 41,506509. Zepke, H. D., Heinz, E., Radunz, A., Linscheid, M. and Pesch, R. (1978). Arch. Microbiol. 119. 157-162.

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The Alternation of Generations

PETER R. BELL

Department of Botany and Microbiology, University College, London WCI E 6BT, UK

I. 11. 111.

IV.

Introduction. .

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The Universality of Life Cycles.

Essential Features of Points of Change A. Gametogenesis . . . . . . B. Sporogenesis . . . . . . .

The Significant Features of Aberrant Cycles A. Aberrant Cycles in Natural Conditions B. Induced Aberrations in Sexual Cycles .

V.

The Causal Approach to Alternation . . . . . . . . A. General Assumptions . . . . . . . . . . . B. From Gametophyte to Sporophyte in the Lower Plants C. From Sporophyte to Gametophyte . . . . . . .

VI.

General Conclusion

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I. INTRODUCTION The “alternation of generations”, the English rendering of “Generationswechsel”, has fascinated botanists since the 19th century. The observations which gave rise to the term were made by the botanist von Chamisso in 18 15 (von Chamisso, 1975) on collections of the tunicate Sulpu gathered while he was becalmed in the Atlantic at the beginning of a Russian exploratory Advancesin Botanical Research Vol. 16 ISBN 0-12-005916-9

Copyright 01989 Academic Press Limited All rights of reproduction on any form reserved.

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voyage around the world. Chamisso noted that the life cycle of Sulpa consisted of alternating generations of oozoids and gastrozooids. Both, however, are now known to be diploid; only the gametes (produced by the gastrozooids) are haploid. “Generationswechsel” was probably brought into botanical terminology by Hofmeister (1851), particularly in relation to the archegoniate plants. Although the archegoniate cycle is, like that of Salpa, biphasic, the two phases normally differ in chromosome number. Nevertheless, Hofmeister’s parallel was justified since the nuclear aspects of the land plant cycle were not recognized until the end of the 19th Century (Overton, 1893; Strasburger, 1894). Much has been written about the alternation of generations of land plants, but attention has been directed principally to its likely evolution (e.g. Graham, 1985), and the selective forces which have moulded its form. Conversely the problem of the physiological events within the plant which drive it through the cycle has attracted little attention. This neglect is partly accounted for by the difficulty of subjecting the cycle to experimental treatments able to give unambiguous results, and partly by the lack of techniques to investigate the intimate events in the cells in which the change in the form of growth is taking place. Nevertheless, sufficient is now known about the gametogenous and sporogenous regions of plants, and of aberrant cycles, to justify constructive speculations about the causal aspects of the cycle.

11. THE UNIVERSALITY OF LIFE CYCLES Examples of life cycles are found at all levels of the Plant Kingdom. As knowledge of life cycles increases, particularly of the microalgae, it may emerge that some form of cycle is the normal accompaniment of photoautotrophic life. Amongst the prokaryotes a well-defined cycle is shown by Nosroc (Lazaroff and Vishniac, 1961). A heterocystous generation alternates with a sporogenous, the transition from the former to the latter being lightdependent. A number of cyanophytes produce minute reproductive cells (baeocytes) by a rapid succession of cell cleavages, and their subsequent development is very suggestive of some form of cycle (Fay, 1983). It is not known whether prokaryotic cycles are regularly accompanied by any change in the number of copies of the genome in the nucleoid. No form of sexual reproduction has been detected in the Cyanophyta. Life cycles are well established in the eukaryotic algae, even in those that are unicellular. Amongst the unicellular green algae, the cycle of Chlamydomonas has been particularly well studied. A medium poor in nitrogen induces gametic behaviour. Different mating types are characterized by complementary agglutins coating their flagella (Adair, 1985; Crabbendam et al., 1986; Samson et al., 1987). Copulation, which begins by association of the tips of the flagella, leads to the formation of a resting zygote. Meiosis takes place on

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germination, and the haploid phase is restored in the production of four meiospores. Amongst the multicellular Chlorophyta, Ulva displays a life cycle in which haplophase and diplophase are morphologically identical. The production of zoospores is preceded by meiosis. The fusion of the gametes is similar to that observed in Chlamydomonas, but the zygote germinates without meiosis, and a diploid plant is formed. Some species of Cladophora show a similar cycle. A clear morphological distinction between motile male gametes and sessile female gametes is also found in the Chlorophyta, the genera Coleochaete and Chara providing striking examples of perfect oogamy. In each the egg cell is either initially or subsequently ensheathed in somatic cells. Significantly, it is also these algae which show ultrastructural and metabolic features (in relation to the photo-oxidation) which are more like those of land plants than of other green algae (summarized in Graham (1985)). The gametophytic phase in oogamous cycles may be dioecious (as in Coleochaete scutata), but there are no reports of morphological differences between the zoospores giving rise to the two sexes. The Phaeophyta and Rhodophyta also show many examples of life cycles. That of Dictyora parallels the cycle of Ulva, except that Dictyota is oogamous. The cycles of some Rhodophyta (e.g. Polysiphonia) are particularly complex and involve three distinct phases. Nevertheless, these complex cycles are not in principle different from those seen in the Chlorophyta. The sexual cycles of all land plants are oogamous. The gametophytic phase of the lower archegoniate plants may be dioecious with no well-defined differences in the size of the spores giving rise to the two sexes. In the moss Macromitrium, and in the heterosporous pteridophytes and all seed plants, the sex of the gametophytes is firmly correlated with differences in spore size, or the manner in which the spores are generated. Life cycles in the eukaryotic photoautotrophs are marked by two conspicuous events, gametogenesis and sporogenesis, each associated with a point of change in the cycle. Close investigation of these phenomena may therefore reveal the factors which control the cycle. Further, if there is evolutionary continuity in the life cycles of the land plants and their algal ancestors, the essential causal features of gametogenesis and sporogenesis should be recognizable at all levels of advancement. Although the information from algal sources is limited, a comparative review will facilitate the subsequent discussion.

111. ESSENTIAL FEATURES OF POINTS OF CHANGE A. GAMETOGENESIS

1. Algae Zsogamous forms. In flagellated unicellular algae, differences between the sexual and the asexual state are probably more extensive than is at first evi-

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dent. In Chlamydomonas, for example, production of the agglutinins which bring about the adhesion of the flagella preparatory to syngamy involves the activation of genes otherwise quiescent (Forest, 1987). The electron microscope has revealed not only features peculiar to the gametes, but also differences between gametes of complementary mating strains (Martin and Goodenough, 1975). In general, the chromatin of gametes is more condensed than that of somatic nuclei, but it is not known whether this is a feature affecting the nuclei of the two mating strains equally. The gametes of Ulva (Briten, 1971) probably show features similar to those of Chlamydomonas. Oogamous forms. The comparatively gross difference between the gametes which characterizes oogamous cycles involves reduction in the somatic features of the male gamete. In Oedogonium, for example, the spermatozoid, about 20 pm in length, is almost non-photosynthetic (Pickett-Heaps, 1975). The nucleus is reduced in volume, the chromatin is uniformly condensed, and no nucleus can be recognized (Hoffman, 1973). The nucleus of the motile male gamete of Fucus (Phaeophyceae) has similar features (Brawley et al., 1976a). In the Rhodophyta the spermatium of Corallina lacks intact plastids, and the chromatin is in a contracted form suggestive of an arrested mitosis (Peel and Duckett, 1975). The ultimate in specialization amongst algal male gametes is reached by the spermatozoid of the Charales (Chlorophyta). It is an elongated cell, about 60pm in length, containing a linear nucleus. The mitochondria lie at the anterior end in association with the flagella, and the. rudimentary plastids are confined to the tail. The chromatin is again dense, and no nucleolus can be detected (Pickett-Heaps, 1968; Turner, 1968). A striking feature of oogenesis in the green algae is the extent to which this involves unequal divisions. In Oedogonium, for example, the nucleus of the oogonium mother cell divides, but the bulk of the cytoplasm remains with one cell (which becomes the oogonium). The residual cytoplasm and sister nucleus are cut off as a small suffultory cell (Pickett-Heaps, 1975). In Bulbochaete hiloensis, primary and secondary suffultory cells are cut off in sequence (Pickett-Heaps, 1975), and the cytoplasm, which would with equal divisions have been distributed between three cells, remains principally with the oogonium. A comparable situation is found in the Charales (PickettHeaps, 1975). A strikingly unequal division cuts off a small basal cell as the egg is formed. In all the species the development of the egg protoplast involves considerable plasmatic growth, resulting in a several-fold increase in volume. The cytoplasm is characteristically rich in ribosomes, lipid droplets and starch. Mitochondria and small vesicles, many of the latter in Oedogonium of the “coated” kind (Hoffman, 1973), are also conspicuous, but microtubules are not prominent. The nucleus expands and its volume becomes much greater than that of the sperm nucleus (Hoffman, 1971). The chromatin is finely dispersed and the nucleolus enlarged, lacunate, and often accompanied by small

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spherical bodies 0.60.8 pm in diameter (Hoffman, 1971). Scattered throughout the nucleoplasm in both Bufbochaete (Retallack and Butler, 1973) and Oedogonium (Hoffman, 1973) are numerous small aggregates of electronopaque material. The egg cell of Fucus shows similar features (Brawley et al., 1976a). Similar aggregates, with an affinity for the basic stain Toluidine Blue, appear outside the nucleus following fertilization (Brawley et al., 1976b). In Pofysiphonia (Rhodophyta) the egg (carpogonial) nucleus is again enlarged, reaching a volume about five times that of nuclei of neighbouring carpogonial branch cells (Broadwater and Scott, 1982). In some instances the nucleus of the egg cell has been seen connected by a narrow channel with a large vesicle bounded by two membranes lying towards the trichogyne. The contents of the vesicle, although in continuity with the nucleoplasm, lack structure and are almost uniformly electron-transparent. In algae generally the wall of the virgin oogonium does not appear to be notably thickened, and egg cells seem devoid of any conspicuous lipidic layers coating the plasmalemma. Nevertheless, there are indications of some form of isolation of the site of oogenesis from contiguous somatic cells. In Chara, for example, the chloroplasts of the egg cell become cup-shaped and the thylakoids disrupted by the accumulating starch. Those in the cells sheathing the oogonium remain unaffected by these striking changes within the developing gamete (Pickett-Heaps, 1975). 2. Bryophytes and Homosporous Pteridophytes Spermatogenesis. Spermatogenesis in the bryophytes and pteridophytes has much in common, and provides the only instance in land plants in which centrioles appear in the cytoplasm. They are differentiated in association with a centrosome (liverworts) or blepharoplast (mosses, pteridophytes, and zooidogamous gymnosperms), and subsequently function as the basal bodies of flagella. With few exceptions the nucleus of the differentiated gamete is elongated, and its chromatin condensed and without recognizable nucleoli. The skeleton of the gamete is provided, as in the male gametes of the Charales, by a ribbon of microtubules appressed to the nucleus. This ribbon originates in a multilayered structure (MLS) at the anterior end of the gamete. Mitochondria also tend to lie in the anterior part of the gamete (at least one associated with the MLS), and the plastids (which frequently accumulate starch and lose ordered thylakoids) towards the posterior. Plastids and other cytoplasmic components are often shed in a terminal vesicle from the motile gamete. The papers of La1 and Bell (1975), Duckett et al. (1983) and Sheffield and Bell (1987) contain reviews of the differentiation of the male gametes of the mosses, liverworts and pteridophytes respectively. Oogenesis. The female gametes of the bryophytes are less well investigated than those of the male. The egg cell of both liverworts and mosses lies at the base of the canal of the archegonium. Its formation is preceded by two

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unequal divisions, the first yielding the central cell and the neck canal cell initial, and the subsequent division of the central cell yielding the egg cell and ventral canal cell. The cytoplasm, which is increasing throughout these divisions, remains predominantly with the lower cell and becomes the cytoplasm of the egg. Further plasmatic growth results in the egg protoplast becoming conspicuously large, and the cytoplasm well furnished with ribosomes and organelles. Small aggregates of granular electron-opaque material, about 150nm in diameter and with a texture similar to that of the nucleolus, are scattered in the cytoplasm of the egg cells of Sphaerocarpus (Diers, 1965) and Physcomitrium (La1 and Bell, 1977). Numerous vesicles are also a feature of the egg cytoplasm. At maturity the egg cell becomes separated from the wall of the archegonial chamber by a zone of hydrated mucilage. In Physcomitrium there is convincing evidence that this mucilage is expressed from small vesicles which open at the plasmalemma (La1 and Bell, 1977), and this may be the situation in bryophytes generally. There is no indication of a special lipidic or other membrane around the egg cells of bryophytes so far examined (Sphaerocarpus (Diers, 1965); Marchantia (Bell, 1975; Zinsmeister and Carothers, 1974); Fossombronia (Bajon-Barbier, 1977); Philonotis (Bell, unpublished); Mnium (Barbier, 1972); Physcomitrium (La1 and Bell, 1977)). During maturation of the egg cell the nucleus expands and the chromatin becomes dispersed. The prominent nucleolus is often associated with “nuclear bodies”, small aggregates of nucleolus-like material. These have been referred to as “micronucleoli” (Bajon-Barbier, 1977), but this is illegitimate since they have never been demonstrated to contain RNA, although their affinity for uranium stains does indicate acidity. The nucleus itself becomes lobed in the mature egg, often very strikingly (as in Mnium (Barbier, 1972)). In addition, in Sphaerocarpus, Marchantia (Fig. 1 ) and Fossombronia the envelope of the nucleus is extended in the form of sheets which penetrate deeply into the cytoplasm. Although the connection with the main body of the nucleus is often very narrow, in Sphaerocarpus it could not be conclusively demonstrated that the sheets became detached (Diers, 1965). This is probably also true of the nuclear extensions of Marchantia (Zinsmeister and Carothers, 1974) and Fossombronia (Bajon-Barbier, 1977). In the ferns, the most studied of the homosporous pteridophytes, oogenesis can also be regarded as beginning with the formation of the primary cell of the axial row of the archegonium. Two unequal divisions cut off smaller cells towards the neck of the archegonium, the cell remaining at the base becoming the egg cell. A substantial amount of cytoplasm is generated during this sequence, most of which is retained by the egg cell. The initial stages of oogenesis are accompanied by an accelerating synthesis of RNA and protein (Fig. 2). Subsequently, in mid-sequence protein synthesis falls to a low level, but RNA synthesis continues into the newly formed egg cell. Since these results were based upon quantitative autoradiography following pulse labelling with

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Fig. I Marchanris polymorpho. Section of part of a maturing egg cell showing the nuclear protrusions(*). N, nucleus. x 45 OOO. Inset Thick section of the archegonium from which the h e sectionwas taken. The egg cell (arrow) lies in fluid at the base of the archegonium. x 680. I

tritiated widine, it is possible that the apparent cessation of incorporation in the maturing egg may be a consequence of the nucleoside failing to reach the gamete, now becoming an isolated cell. The cytoplasm of the central cell precedmg the egg is characterized by clusters of small vesicles, many suggestive of degenerating mitochondria and plastids (Bell P. R., 1969). The view that the vesicles represent a phase of limited autophagy is strengthened by the vesicles being associated with acid

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PETER R. BELL 2

I

3

4

6

RNA

Fig. 2. Pteridium aquilinum. A comparison of the amounts of ribonucleic acid and protein synthesis during oogenesis. I , 2. growth of the primary cell; 3, formation of the central cell; 4,5, 6, formation and maturation of the egg. Based on pulse-labelling and quantitative autoradiography. From Cave and Bell (1 974a).

phosphatase (Tourte, 1970), a marker of lysosomal activity. Subsequently these vesicles discharge at the plasmalemma, resulting in the mature egg being enveloped in an extra lipidic layer (Cave and Bell, 1974b). During maturation of the egg cell the nucleus becomes conspicuously larger and irregular in outline. The chromatin is well dispersed, but the nucleolus is very prominent and often shows structural differentiation. Nuclear bodies are frequent in the nucleoplasm. Although they resemble micronucleoli, and have a strong affinity for the uranyl ion (Bell, 1983a), there is no evidence that these bodies contain RNA or DNA. Similar bodies in the cytoplasm also appear to lack nucleic acids (Bell and Pennell, 1987). It seems beyond doubt that they consist principally, if not entirely, of acidic protein. In the egg cells of certain ferns, but not all (Bell, 1986), maturation of the egg cell is accompanied by a remarkable interpenetration of nucleus and cytoplasm. In Pteridium the nuclear protrusions take the form of vesicular blebs (bounded by both membranes of the nuclear envelope) or hooded sheets (Bell and Duckett, 1976; Fig. 1). In Dryopteris (Bell, 1974) and Histiopteris (Bell, 1980) the sheet-like protrusions are folded and interconnected, giving formations of remarkable complexity. There are clear indications, particularly in Pteridium, that the nuclear bodies enter the vesicular protrusions, and from there the material finds its way into the cytoplasm. There is, how-

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ever, no conclusive evidence that these protrusions open and release the bodies into the cytoplasm. The material seems to leave the nucleus by some form of secretion (Bell and Pennell, 1987). The cytoplasm of the mature egg cell is well furnished with mitochondria and plastids, the latter being irregular in shape and often, following conventional fixation, having very indistinct boundaries (Bell, I983b). The matrices are commonly dense and the internal lamellae rudimentary. High-resolution autoradiography reveals that both mitochondria and plastids contain notable amounts of DNA. Pulse-labelling indicates that incorporation of tritiated thymidine is directly into the DNA within the organelles (Sigee and Bell, 1971; Sigee, 1972). Microtubules do not seem to be a feature of the egg cells of more recent ferns, but they are not uncommon in the egg cell of Todea, representative of an ancient family (Bell, 1986). 3. Heterosporous Pteridophytes and Seed Plants Spermatogenesis. There is little difference in principle between spermatogenesis in heterosporous and homosporous ferns. Marsilea has been studied in greatest detail (Myles and Bell, 1975; Myles and Hepler, 1982). The mature spermatozoid, although larger, is constructed in the manner of that of Pteridium. The same holds for the large spermatozoids of the zooidogamous gymnosperm Zamia (Norstog, 1968, 1974), and probably also of Ginkgo, although this awaits detailed examination. In the conifers (including Taxus) the male gametes are much less elaborate than in the zooidogamous archegoniates. They consist generally of a pair of nuclei in the persistent cytoplasm of the mother (spermatogenous) cell (e.g. Taxus (Pennell and Bell, 1988) and Agathis (Kaur and Bhatnagar, 1984)). There is no detectable provisions for propelling the sperm nuclei into the archegonium, although actin may be involved. In the flowering plants, the sperms while in the pollen tube and during discharge are distinct cells. Each is enclosed in its own plasmalemma, and the pair are surrounded by the plasmalemma of the vegetative cell. In a number of dicotyledons one of the sperm cells is connected with the convoluted vegetative nucleus. The complex formed by the two sperm cells and vegetative nucleus is referred to as the “male germ unit” (e.g. Brassica (McConchie et al., 1985) and Petunia (Wagner and Mogensen, 1988)). Although in the grasses the two sperm cells appear to be clearly separate, they become associated with the vegetative cell on germination, and the association persists during the growth of the tube (Mogensen and Wagner, 1987). The two sperm cells are not always identical in content. In Plumbago, for example, one sperm cell retains most of the mitochondria, and the other the plastids. The cell rich in plastids fuses preferentially with the egg cell (Russell, 1985). Oogenesis. Oogenesis in the heterosporous archegoniates follows a course similar to that seen in the homosporous, but with some significant differences. The archegonia are simpler with less development of the neck. The

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vesicular phase early in oogenesis appears to be absent and correspondingly no additional lipidic layer has been observed around the egg cell. The interpenetration of nucleus and cytoplasm, so striking a feature in some homosporous ferns, has never been seen in heterosporous forms (Tourte et al., 1971; Robert, 1972). The cytoplasm is rich in organelles, the plastids being commonly dedifferentiated and often curiously shaped (as in Selaginella (Robert, 1972)). In the cycads the egg cells are particularly large, the protoplast in Zamia, for example, reaching a diameter of 3 mm, and its nucleus at least 0.5 mm (Konar and Moitra, 1980). During maturation the Feulgenpositive material in the nucleus contracts to a small globule, but chromatin elsewhere may be too finely dispersed to give a detectable stain. The nuclear surface becomes undulate, and refractive granules, with no detectable Feulgen staining, are seen to stream from its surface into the cytoplasm (Bryan and Evans, 1956). No cytochemical or ultrastructural details of this phenomenon are yet available. In the conifers (including Taxus) oogenesis follows the same course as in the zooidogamous gymnosperms (Konar and Moitra, 1980). In some instances (e.g. Taxus (Pennell and Bell, 1987a)) it is not clear whether the nucleus of the central cell divides, in which case the central itself could function as the gamete. Alternatively, division may take place, but the upper ventral canal nucleus may be resorbed so quickly that it has escaped detection (Konar and Moitra, 1980). The mature egg cells are characterized by a wellordered cytoplasm. An outer zone contains whorls of endoplasmic reticulum and complex inclusions believed to be derived from plastids (Pennell and Bell, 1987a; Camefort, 1966), and long regarded as “protein bodies”. The large nucleus is surrounded by an inner zone of lipid globules and an intermediate zone of mitochondria. Amongst the mitochondria are small uraniophilic bodies (in some conifers clearly Feulgen-positive (Konar and Moitra, 1980)) about 600 nm in diameter. These may represent mitochondria which have lost their internal structure but have retained their DNA (Pennell and Bell, 1987a). Recognizable plastids are conspicuously absent. No recent information is available concerning the egg cells of Ephedra, Gnetum and Welwitschia. The egg cells of the flowering plants tend to be less complex than those of the archegoniates. They are usually larger than the accompanying cells at the micropylar end of the embryo sac, and the nucleus is swollen and barely Feulgen-positive. Although Woodcock and Bell (1968a) were able to show by means of UV microspectrography that DNA was present in the cytoplasm of the egg cell of Myosurus (whereas none was detectable in the cytoplasm of adjacent nucellar cells), the cytoplasm is comparatively poor in mitochondria and plastids (Woodcock and Bell, 1968b). This seems to be a feature of the egg cells of flowering plants generally (Kapil and Bhatnagar, 1981; You and Jensen, 1985). Nucleocytoplasmic interaction of a physical kind has not been observed, and notable cytoplasmic inclusions appear to be lacking.

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B. SPOROGENESIS

1 . Algae Detailed studies of the spore mother cells of eukaryotic algae are remarkably few. Hopkins and McBride (1 976) were able to show by Feulgen microspectrophotometry that the amount of DNA in the zygotic nucleus of Coleochaete scutatu reached eight times the unreplicated haploid level, indicating two rounds of DNA replication before meiosis. Meiosis itself and the differentiation of the meiospores of C. pufvinata has been followed in the electron microscope, but unfortunately with few details of the cytoplasm and no cytochemical data (Graham and Taylor, 1986). The most complete descriptions available are of tetrasporogenesis in the Rhodophyta. In Dasya, for example, the frequency of ribosomes in the tetrasporangium diminishes conspicuously during prophase I, and aggregates of electron-opaque granules, which stain intensely with basic dyes, appear in the cytoplasm during diplotene (Broadwater et al., 1986). It is unfortunate that few details are available of meiosis in the oospore of the Charales. Although a tetrad of nuclei is formed, three nuclei are resorbed (a feature also of the germinating zygote of Spirogyra). Study of this remarkable feature has probably been hampered by the extreme difficulty of fixing the mature egg cell and zygote of the Charales. 2. Bryophytes and Homosporous Pteridophytes Although comprehensive studies of sporogenesis in bryophytes are few, current knowledge points to the sporocytes of both liverworts (Horner et al., 1966; Kelley and Doyle, 1975) and mosses (Brown and Lemmon, 1980) being surrounded by conspicuous polysaccharide walls with a fibrillar texture. The cytoplasm of the sporocyte and subsequent spore mother cell is rich in ribosomes (Horner et al., 1966; Eyme and Suire, 1971; Brown and Lemmon, 1980), and in Riccardia has a corresponding strong affinity for basic stains (Homer et al., 1966). No diminution in ribosome frequencies or basophilic staining becomes apparent until the formation of the spores (EymC and Suire, 1971; Horner et al., 1966). The behaviour of the mitochondria during sporogenesis is unremarkable, but the reduction in the number of plastids, especially in mosses, has attracted considerable attention (Paolillo, 1969; Jensen and Hulbary, 1978). This reduction, leading in some instances to only one being present in the sporocyte, is probably a consequence of division of the plastids failing to keep pace with mitosis in the development of the sporogenous tissue, although reduction by fusion has also been suggested (Jensen and Hulbary, 1978). Where a single plastid is present in the sporocyte, it divides into four at meiosis, one passing into each newly formed spore. The situation in the liverworts is less regular (Ramsay, 1983). Sporogenesis in the homosporous pteridophytes has been studied most

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extensively in the ferns. Noteworthy features (reviewed in Sheffield and Bell (1987)) are the occlusion at an early stage of all plasmodesmata between the tapetum and the sporogenous cells, and the thickened walls which form around the spore mother cells. During prophase of meiosis there is loss of basophilia from the cytoplasm and a sharp reduction in the frequency of ribosomes. In mid-prophase, balloon-like invaginations of the inner membrane of the nuclear envelope penetrate the nucleoplasm. The “nuclear invaginations” detected at pachytene and subsequently in Psilotum (Gabarajeva, 1984) are probably of like origin. Small aggregates of material with a texture similar to that of the nucleolus are present in the cytoplasm. These aggregates disperse in the cytoplasm of the young spores coincident with an increasing frequency of ribosomes. Also striking at this time is a brief phase in which narrow tubular extensions of the nucleus penetrate the cytoplasm, often running very close to organelles but without evident connection. In Anemia (Schraudolf, 1984) this phase of nucleocytoplasmic interaction takes the form of nuclear invaginations, involving both membranes of the envelope, carrying finger-like columns of cytoplasm into the nucleus. These invaginations often terminate in a swelling, associated internally .and externally with electron-opaque material. In sporogenesis generally in the homosporous vascular archegoniates the plastids have lost much of their internal structure by the end of prophase, but it is progressively regained during the development of the spores. In Lycopodium there are indications of a degeneration of a proportion of the mitochondria and plastids in the mother cell (Pettitt, 1978), but this does not appear to be general in the pteridophytes. In some species of pteridophytes which are usually regarded as homosporous, the spores nevertheless fall into two size classes. A notable example is the fern Platyzoma. Preliminary examinations show that, although there is some variation withing sporangia, the large and small spores are produced separately and in different numbers (Tryon, 1964). Sporogenesis has not yet been investigated in detail, but it appears that omission of one or two of the mitoses in the sporogenous lineage results in fewer spore mother cells and larger spores. There are no indications of regular degeneration of spore mother cells or meiotic products. 3. Heterosporous Pteridophytes and Seed Plants Microsporogenesis. The principal contribution by modern techniques to knowledge of microsporogenesis in heterosporous pteridophytes concerns Azolla. There are close similarities to homosporous sporogenesis, including the formation of a thickened wall around microspore mother cells and the coincident breaking of all plasmodesmatal connections with the tapetal cells (Herd et al., 1985). Subsequently, as the nucleus of the mother cell enters prophase, the density of the cytoplasm diminishes. Isolation of the mother cell is also a feature of the conifers. In addition, studies of developing microsporangia reveal a second layer, the peritapetal

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membrane (Dickinson, 1970a), which surrounds the whole spore sac, including the tapetum. Since this membrane resists acetolysis and probably consists of sporopollenin, it may reinforce the isolation of the developing spores from all but simple nutrients from the parent plant. In other respects, microsporogenesis in conifers (reviewed by Moitra and Bhatnagar (1982)) has many resemblances, including the formation of nuclear vacuoles in prophase (Sheffield et al., 1979), to sporogenesis in homosporous pteridophytes. It should be noted, however, that prophase of meiosis is often prolonged (Anderson et a/. 1969; Owens and Molder, 1971). In Taxus, where prophase lasts about 4 weeks, there is no dramatic fall in cytoplasmic RNA in the mother cells during this time (Pennell and Bell, 1987b). This is possibly also the situation in other conifers with extended meioses. Dickinson (1981), for example, comments on the relatively small decline in cytoplasmic RNA during prophase in Pinus. A remarkable feature of the newly formed pollen grains of Pinus (Dickinson and Bell, 1970) and Podocarpus (Aldrich and Vasil, 1970) is the invagination of the nuclear envelope in a manner similar to that seen in Anemia. In Pinus the electron-opaque material within the invagination has been shown to be rich in RNA (Dickinson and Potter, 1975), and the material in the nucleus surrounding the invagination to be chromatin (Li and Dickinson, 1987). The extensive investigations of microsporogenesis in flowering plants reveal a situation similar in essentials to that in conifers. Isolation of the microspore mother cells by thickened (and often callosed) walls appears to be general. Later in sporogenesis an acetolysis-resistant peritapetal membrane, corresponding to that in conifer microsporangia, has been detected around the tapetum and sporogenous tissue in Cosmos and some other Compositae (Heslop Harrison, 1969). A similar membrane occurs in Brassica, but not in Petunia or Lilium (Dickinson, personal communication). A striking fall in cytoplasmic RNA during prophase has been observed in a number of species, but it is not known whether this is also a feature of those species in which meiosis is prolonged (e.g. Trillium erectum, in which meiosis occurs naturally at 6 6 ° C and lasts several weeks (Sparrow et al., 1955)). In Lilium the fall is now known to involve both ribosomal and messenger RNA (Porter et al., 1984). Nucleolar activity is also conspicuous before metaphase I, and bodies regarded as micronucleoli are frequent in the nucleoplasm (Dickinson and Heslop Harrison, 1976). Also at this time a tendency for the inner membrane of the nuclear envelope to invaginate into the nucleoplasm has been seen in Lycopersicon (Sheffield et al., 1979) and Datura (Sangwan, 1986). Prominent in the cytoplasm of Lilium throughout meiosis are regions of cytoplasm bounded by two or three membranes, and also, following anaphase I, bodies strikingly like nucleoli (“nucleoloids”) (Dickinson and Heslop Harrison, 1976). Both disperse in the young spores, the dispersal being associated with a return of ribosome frequencies to pre-meiotic levels.

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Neither the source nor the composition of the nucleoloids is yet clear, and it would not be safe to assume on present evidence that they contain RNA (Dickinson. 1987). At the tetrad stage there are also indications in Lilium of activity at the nuclear surface. Both blebbing of the outer membrane of the envelope, the blebs containing electron-opaque material, and vesicular extensions of the nucleus itself, bounded by both membranes of the envelope, have been observed (Dickinson, 1971). Also at this time in Lilium, and probably elsewhere, the plastids, which have become wholly dedifferentiated by the end of meiosis, acquire starch and rudimentary internal lamellae (Dickinson and Heslop Harrison. 1970). Megasporogenesis. In the heterosporous ferns, megasporogenesis has been most fully investigated in Marsilea. As the sporogenous cells prepare for meiosis they acquire thick walls, and on entering meiosis show loss of ribosomes (Bell, 1981). Meiosis results in a tetrahedral tetrad of megaspores indistinguishable ultrastructurally from each other (Bell, 198 1). Nevertheless, before the spores separate, one spore begins to degenerate, followed by two more as the tetrad opens (Bell, 1985). Of the surviving megaspores liberated into the invasive tapetum, one soon establishes dominance, and it alone comes to maturity. In the maturing megaspore the surface of the nucleus is particularly active. Tubular extensions, each connected to the main body of the nucleus by a narrow channel, penetrate far into the cytoplasm. Although they often run close to mitochondria and plastids, sometimes making contact with their envelopes, continuity of contents has never been observed. The cytoplasm of the maturing spore, lying around a central vacuole, is well furnished with ribosomes and organelles. Occasionally, large vesicle-like extensions of the whole nucleus containing only electron-translucent material have been observed within the central vacuole (Bell, 1985). In Seluginella, megasporogenesis is altogether less regular. The mother cells in the megasporangia are fewer than in the microsporangia. Some, with a cytoplasm less rich in RNA, degenerate (Horner and Beltz, 1970). In addition to degeneration of megaspore. mother cells, those remaining may produce megaspores of different sizes, only the larger coming to maturity (Pettitt, 1977). The differences in behaviour can be related to gradients in the cytoplasm of the mother cell. In Isoetes there are similar differences in the number of mother cells in the mega- and microsporangia, but all the megaspores come to maturity. In I. engelmanni each megaspore inherits a large proplastid which, by a remarkable process of budding, restores the plastid population in the maturing megaspore (Pettitt, 1976). In gymnosperms in general the megaspore mother cell appears to be isolated from the nucellus by a thickened wall lacking plasmodesmata. Information about meiosis and the accompanying events in the cytoplasm is limited. In the megaspore mother cell of Ginkgo, Stewart and Gifford (1967) detected a marked polarization in the distribution of the organelles, most of the mito-

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chondria and plastids being confined to the chalazal hemisphere. A similar situation is found in Taxus (Pennell and Bell, 1987a). Also in Taxus most of the ribosomes seem to be conserved during meiosis, but significant cytochemical information corresponding to that relating to prophase in the microsporangia (Pennell and Bell, 1987b) is lacking. In extinct gymnosperms, megaspores were probably formed in tetrahedral tetrads (Pettitt, 1969), but in living species meiosis results in a linear tetrad, or a T-shaped tetrad in which the upper diad has divided transversely to the axis of the ovule. Tetrahedral arrangements are, however, sometimes encountered in conifers in which there are several megaspore mother cells in the nucellus (e.g. Sequoia (Looby and Doyle, 1942)). Normally the spore in the chalazal position is alone capable of further development. In Taxus (and probably, but not certainly, elsewhere) this is also the spore which retains most of the cytoplasm derived from the mother cell. Whether this is a sufficient condition for its survival is not known. In flowering plants the megaspore mother cell, surrounded by a thickened and often callosed wall, is in general characterized by a cytoplasm with dedifferentiated mitochondria and plastids and few ribosomes (Kapil and Bhatnagar, 1981). Megasporogenesis has been studied in greatest detail in Lilium (Dickinson and Potter, 1978). The changes in the cytoplasm parallel those seen on the male side, including pre-metaphase nucleolar activity, and the subsequent appearances of nucleoloids in the cytoplasm. Regions of cytoplasm enclosed in whorls of membrane are also conspicuous. Although in Lilium these are regarded as protecting a proportion of the cytoplasm from the partial autophagy evident elsewhere, Schulz and Jensen (1981) find that the membranes surrounding similar bodies in the megaspore mother cell of Capsella are rich in acid phosphatase, a marker of lysosomal activity. During prophase, vesicular extensions of the nucleus are found in Capsella (Schulz and Jensen, 1981), but in Myosurus these are a feature of the developing megaspore (Woodcock and Bell, L968b). The extensions recall those seen in the developing megaspores of Marsilea, and, as there, occasionally contain internal membranes. Coincident with the nuclear activity in Myosurus, the cytoplasmic DNA (as determined by UV microspectrography) begins to increase, reaching a maximum in the two-celled embryo-sac (Woodcock and Bell, 1968a). In species with monosporic embryo-sacs the mitochondria and plastids are often concentrated in the chalazal region of the megaspore mother cell, resulting in an unequal division between the spores. This has been held to account for the promotion of the chalazal spore, but in Myosurus (Woodcock and Bell, 1968a) and some other species (Kapil and Bhatnagar, 1981) there is no evident inequality in the distribution of the organelles. In Capsella (Schulz and Jensen, 1981) and some Orchidaceae (Rodkiewicz and Bednara, 1976) the chalazal region of the wall of the mother cell and of the subsequent surviving megaspore becomes labyrinthine, leading to the suggestion that

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this spore alone receives nutrients adequate for development. This view is strengthened by the presence in Oenothera, in which the micropylar megaspore survives, of plasmodesmata in the corresponding micropylar portion of the wall of the mother cell (Jalouzot, 1978). Although the usual terms “microspore” and “megaspore” have been used in this chapter it should be noted that megaspores in seed plants are often smaller than the microspores (Doyle, 1953). “Androspore” and “gynospore” would be a more accurate terminology.

IV. THE SIGNIFICANT FEATURES OF ABERRANT CYCLES A. ABERRANT CYCLES IN NATURAL CONDITIONS

1. Algae

In the algae the reproductive cells appear to be particularly labile. In Chlumydomonas, for example, the gametes can revert to somatic behaviour. A similar situation is found in Ulva and the brown alga Ectocarpus. In Oedogonium the oogonia may develop parthenogenetically, and a cycle continue without meiosis. In Chara crinita, although the nuclear relationships are not clear, the egg cell forms an oospore which develops without fertilization, and most populations appear to maintain themselves by a parthenogenetic cycle. The life cycles of many algae change readily in response to fluctuating environmental conditions. In some instances perfect cycles are so infrequent that the relationship between gametophyte and sporophyte has not been recognized, and the two forms have been placed in separate genera. The situation is further complicated by one form sometimes being able to give rise directly to the other (as occurs, for example, in the Halicystis (gametophyte)/Derbesia (sporophyte) complex in the Chlorophyta (Rietema, 1975)). A general review of algal cycles and their deviations can be found in Ettl et al. (1967). 2. Bryophytes and Homosporous Pteridophytes Although many bryophytes propagate themselves readily by means of gemmae or fragmentation, aberrant cycles with a clear relationship to the sexual cycles are unknown in natural conditions. Amongst the homosporous pteridophytes, natural aberrant cycles are also unknown in the lycopods and Equisetum, but are common in the ferns. A familiar example is provided by Pteris cretica. Common to this kind of cycle (first clarified in Dryopteris by Dopp (1939)) is the failure of telophase in the final mitotic division of the sporogenous cell lineage, and the subsequent production of an embryo without gametic fusion. In the sporangia the failure of telophase in the sporogenous lineage results in the nucleus of the spore mother cell containing a doubled number of chromosomes. During the

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formation of this restitution nucleus a transverse wall grows in from the margins of the cell, resembling in the manner of its formation (except for the absence of transverse microtubules) the phycoplast of a dividing algal cell (Fowke and Pickett-Heaps, 1969). The wall may even begin to constrict the nucleus, but at this point it is rapidly resorbed and the nucleus prepares for the prophase of meiosis (Sheffield et al., 1983). Many ferns with this kind of cycle (the so-called “apogamous” ferns) are (in comparison with their sexual relatives) triploid or pentaploid, and the events in the sporangia are variable. The sporangia producing viable spores normally contain 8 spore mother cells, but 4- and 16-celled sporangia also occur. Sporogenesis in these is irregular and the spores largely inviable. The development of the few which germinate has been little studied. In Dryopteris afinis subsp. afinis, a diploid form, 8-celled sporangia predominate (Sheffield et al., 1983). The spores produced in the 8-celled sporangia of the apogamous ferns are larger than those of their sexual relatives (in which the sporangia contain 16 spore mother cells). In Dryopteris, for example, the respective diameters are of the order of 80 pm and 40 pm, indicating an eight-fold difference in volume. The gametophytes of the apogamous ferns mature faster than those of sexual relatives (Whittier, 1970). After passing through a male phase, an embryo is produced directly, without clear demarcation between the tissue of the gametophyte and the cells initiating the embryo (Laird, 1986). In a second form of apogamous cycle, found hitherto only in tropical ferns, there is no synapsis of chromosomes in the prophase of meiosis. The nuclei reform without division. The second division of meiosis is normal and spores are formed in diads with an unreduced chromosome number (Braithwaite, 1964). Many ferns with this kind of cycle have high chromosome numbers (Walker, 1985). The spore output is generally low, and the spores are variable in size. Embryos are produced directly from the gametophytes, but sometimes only after prolonged growth. A number of cycles involving apogamy are also known from cultivated varieties of ferns. Notable examples’are provided by the varieties clarissima Jones and clarissima Bolton of Athyrium Jilix-femina (Farmer and Digby, 1907). In both, gametophytic outgrowths arise aposporously from the soral regions of fertile fronds, the sporangia themselves being abortive. In clarissima Jones the gametophyte bears antheridia and archegonia, but the archegonia are not functional and the embryo arises apogamously from somatic tissue of the gametophyte. Var. clarissima Bolton is quite similar, but the embryo is said to arise by the parthenogenetic development of an egg cell. Unfortunately these varieties are now very rare in cultivation, and it has not been possible to reinvestigate them by modern techniques.

3. Heterosporous Pteridophytes and Seed Plants Parthenogenetic development of egg cells is known in species of Marsilea, Salvinia, Selaginella and Isoetes (Dopp, 1967; Bhardwaja and Abdullah,

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1972; Mahlberg and Baldwin, 1975). Since in some instances whole populations are affected, and microsporangia are either absent or very rare (Bhardwaja, personal communication), they are presumably able to maintain themselves by means of parthogenetic cycles. The nuclear aspects of these cycles are not fully known. In Isoetes, polyploidy is probably involved (Marsden, 1976). Apart from various forms of polyembryony (which can be regarded as a form of vegetative reproduction), gymnosperms provide no known examples of aberrant cycles. Angiosperms, on the other hand, provide many. Parthenogenetic cycles are well represented, for example, in the grasses, Compositae and Rosaceae. In all these instances the female gametophyte either develops aposporously from a somatic cell of the nucellus, and is thus diploid from its initiation, or its origin lies in a modified meiosis which results in a pair of nuclei with unreduced chromosome numbers (Nygren, 1967). In Alchemilla some archaesporial cells may reach anaphase of meiosis I, but development does not proceed further. The functional embryo-sacs are either diplosporous or aposporous (Izmailow, 1986). In some flowering plants with apomictic cycles, continued development of the parthogenetic embryo depends upon pollination. Although pollination may do nothing more than provide a general stimulus necessary for the development of the seed and fruit, its function is sometimes more precise. In Panicum maximum, for example, one of the sperm cells fuses with the central cell to form an endosperm nucleus (Warmke, 1954). Endosperm and parthenogenetic embryo then develop together as in a normal seed. B. INDUCED ABERRATIONS IN SEXUAL CYCLES

1. Algae Many of the variations seen in life cycles in nature have been reproduced in culture, and the conditions inducing the aberrations identified (Ettl et al., 1967). Reports of wholly new forms produced experimentally are few. Mainx (1931) was able to obtain a race of Oedogonium plagiostomum (Chlorophyta) with giant cells by germinating fertilized oogonia without preliminary chilling. In several instances the zygote grew out as a single cell and gave rise to a massive filament. Although the supporting cytology is lacking, it seems likely that in the experimental conditions meiosis failed and the growths obtained were diploid. The filaments produced zoospores (with diameters of 40 pm as opposed to 20 pm) and oogonia, but antheridia were very rare. Unfertilized oogonia ultimately degenerated and showed no tendency to parthenogenetic development, despite parthenogenesis being not uncommon in the Oedogoniales in nature. In the Rhodophyta, Waaland (1978) was able to fuse protoplasts from somatic regions of male and female plants of Grifithsiu. These parasexual heterokaryons (the nuclei did not fuse) gave rise to growths having the char-

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acteristic form of tetrasporangial branches, although no viable tetraspores were produced. When the fusion was restricted to protoplasts from the male, or from the female plants, the filaments produced solely the correspdnding sexual reproductive structures, and tetrasporangial features were absent. In the Phaeophyta it has been claimed that treatment of egg cells of Fucus with low concentrations of fatty acids leads to parthenogenesis (Overton, 1913), but these results lack confirmation (Evans et al., 1982). 2. Bryophytes and Homosporous Pteridophytes Bryophytes were the first group of archegoniates in which it was demonstrated experimentally that not only the spores, but also cells in other regions of the sporophyte, would give rise to gametophytic growths (Pringsheim, 1876; Stahl, 1876). Subsequently it was observed that gametophytes generated in this way often bore sporogonia apogamously. In some instances the appearance of sporogonia was encouraged by dryness of the medium, and fluctuations in hydration could lead to bizarre growths in which leaves and sporogonia alternated along the axis of a shoot (see Bauer (1967) for a review of the earlier work). Investigations of the regenerative capacity of young normal sporogonia showed that although the seta would give rise only to protonema, the apical region would regenerate either sporogonia directly, or callus which produced sporogonia on further culture. This difference in response was partiqularly marked in the hybrid sporogonium Funaria x Physcomitrium (Fig. 3). A later discovery was that secondary protonema developed from shoots of naturally-occurring species (and therefore wholly gametophytic in origin) would also develop sporogonia apogamously in culture, particularly if sugar were present in the medium (Lazarenko et al., 1961; Lal, 1961). In Physcomitriumpiriforme, which also behaves in this way, the sporogonia were found to arise from groups of isodiametric intercalary cells initiated by unequal divisions of the normally long protonemal cells (Menon and Lal, 1972). The intercalary cells have a dense cytoplasm containing abundant ribosomes. Some develop labyrinthine walls, but there is no organized interface between the developing sporogonium and the protonemal filament (Menon and Bell, 1981). It is not clear whether the protonema of species with basic chromosome numbers is also capable of behaving apogamously. In all instances hitherto the species which have responded in this way have chromosome numbers which suggest a polyploid origin. In Funaria hygrometrica, which exists naturally as two races (n and 2n), Bauer (1959) found that the protonema of the diploid race produced sporogonia apogamously, but that of the haploid grown in the same conditions did not. The existence of a “sporogonial factor” affecting the readiness with which a gametophyte displays apogamy has been suspected (see Lal, 1984). This may be hormonal. The kinetin-like hormone “bryokinin”, for example, promotes apogamy in Splachnum

Fig. 3. The kinds of regeneration obtainable from the different zones of developing moss sporogonia. A, apical cell and immediately adjacent cells; B,, meristematic region eventually giving rise to the capsule; B,, meristem contributing to the seta, at a later stage forming the apophysis; C, extension zone; D, fully differentiated part of seta; E, foot of a normally developed sporogonium; E,, foot of an apogamously formed sporogonium. The broken lines indicate indefinite continuation of the growth form depicted in the appropriate cultural conditions. From Bauer (1963).

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(Bauer, 1966). The distribution of the factor within a culture may not be uniform. Ripetsky (1980, 1983), working with Portia intermedia, found that protonema regenerated from protoplasts extracted from cells adjacent to the sporogenous cells wholly lacked an apogamous tendency. Protonema regenerated from protoplasts from all other somatic regions of the sporogonium showed frequent apogamy, and the tendency was retained indefinitely in culture. Although the sporogonia of liverworts will also give rise to gametophytes aposporously (Lang, 1901; Burgeff, 1937; Lal, 1984), there are no reports of apogamy. It may be significant that low chromosome numbers, suggestive of the predominance of basic haploidy, are a feature of these bryophytes (Berrie, 1960). Although interest in apospory in ferns was initially concerned principally with those species with apogamous cycles, the ability of young leaves generally to produce gametophytic outgrowths in experimental conditions also became apparent (Goebel, 1907; Lang, 1924). In the experiments of Sheffield and Bell (1981), carried out in defined conditions, small explants of the first leaf of Pteridium sporelings placed on agar medium regularly began to grow out as gametophytes within 3 days (Fig. 4). In these experiments, and in those of Hirsch ( 1975) on Microgramma, sucrose discouraged the aposporous response. Numerous experiments on the induction of apospory in sexual species (Goebel, 1907; Lawton, 1932; Morel, 1963; Sheffield and Bell, 1981; von Aderkas, 1986; Kwa et al., 1988) have shown that the response declines with successive leaves. Although possibly partly a consequence of a thickening cuticle as the form of the leaf becomes more mature, this explanation cannot wholly suffice. Even the delicate prothallus-like outgrowths produced in the soral regions of some forms of Pteridium (possibly a consequence of mites (Whittier, 1966)) cannot be induced to develop into gametophytes in culture (Steil, 1949). Ultrastructural examination of the cells in Pteridium explants changing from sporophyte to gametophyte reveals a rapid resumption of meristematic features. The cytoplasm becomes denser, the ribosomes more numerous, and the mitochondria and plastids, which undergo no dedifferentiation, multiply (Sheffield, 1985). Apogamy can be induced in some pteridophytes by the simple expedient of withholding surface water from cultured gametophytes. Only in a few instances will these outgrowths become well established and produce fertile fronds (Manton and Walker, 1954; Palta and Mehra, 1983). Meiosis is then imperfect and the spores are largely inviable. An extreme form of apogamy is the production of sporangia directly on the gametophyte (Lang, 1929; Lawton, 1932), but again the spores are probably inviable. Numerous experiments on the induction of apogamy in Pteridium (in which the outgrowths achieve only limited development) have been carried out by Whittier and coworkers. The presence of sucrose in the medium (Whittier and Steeves, 1960) and ethylene in the ambient atmosphere (Elmore and Whittier, 1975) pro-

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Fig. 4. Pieridium aquilinum. Low-temperature scanning electron micrograph of the upper surface o f an aposporous explant. 5 days after detachment of the juvenile leaf from the parent plant. Two of the outgrowths (arrows) have already developed two-sided apical cells. x 95. Micrograph supplied by Dr E. Sheffield.

mote the response. There seems to be a tendency for diploid races of fern gametophytes to yield apogamous outgrowths more readily than haploid (Heilbronn, 1932; Whittier, 1966~). Apogamy has also been recorded in ageing cultures of Lycopodium deprived of surface water (Freeberg, 1957). In Equisetum, apogamous outgrowths of clearly sporophytic form have been obtained by treating gametophytes with kinetin (Ooya, 1974).

3. Heterosporous Pteridophytes and Seed Plants Fragments of young leaves of Marsilea, treated in exactly the same way as those of Pteridium, failed to show any form of development (Sheffield and

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Bell, 1981).There are no records of aposporous regeneration in Sefagineffaor Isoetes. It seems that the acquisition of heterospory carried with it loss of the ability to generate gametophytic tissue aposporously. Parthenogenetic apogamy can be induced in Marsifea and other members of the Marsileaceae by culturing megaspores in the absence of microspores (Shaw, 1897; Mahlberg and Baldwin, 1975; personal observations on Marsifeu vestira). Whether this is effective with heterosporous pteridophytes other than the Marsileaceae is not known. Apospory is not reported in gymnosperms, but the apogamous development of plantlets from tissue of the female gametophyte is recorded in cycads (La Rue, 1954; Norstog and Rhamstine, 1967) and in Ephedra (Konar and Singh, 1979). It is conceivable that aberrations of the cycle could be successfully induced in other archegoniate seed plants, but experiments with Ginkgo, using pollen and explants of female gametophyte, have hitherto yielded only callus (Tulecke, 1967). This has been the experience with a number of other gymnosperms (Winton and Stettler, 1974). Induced apospory in the flowering plants concerns principally the nucellus, the site of megasporogenesis, and those species in which there is already a tendency towards ambivalence. In the grass Dichanthium aristatum, for example, both normal and aposporous embryo-sacs are a feature of the regular cycle. The proportions of the two forms of sac can, however, be varied by altering the photoperiod. With the minimum period of photoinduction necessary for flowering the proportion of the aposporous sacs falls significantly (Knox and Heslop Harrison, 1963). Induced aposporous development of a gametophyte from cells in the male lineage appears not to have been observed. The parthenogenetic development of egg cells of flowering plants can be induced in a number of ways. Irradiation of embryo-sacs will in some instances destroy the nucleus of the egg cell, but the cell nevertheless remains viable, Pollination then results in a haploid embryo (Ehrensberger, 1948). The use of irradiated pollen can also lead to haploid embryos (Laccadena, 1974). Haploid embryos have also been obtained by treating pollen with the dye Toluidine Blue (which binds to DNA). The growth of the tube is not prevented, but the sperm nuclei are inactivated (Illias, 1974). Certain aberrant genes, such as the hap gene in barley (Hagberg and Hagberg, 1980) and the “indeterminate gametophyte” (ig) gene in maize (Kermicle, 1969), can also promote parthenogenesis. Finally, in some instances it is possible to raise haploid embryos by direct culture of the egg cell (Zhou and Yang, 1981). A surprising discovery has been the readiness with which pollen grains in suitable cultural conditions will give rise to haploid embryos. The range of plants in which this has been accomplished is impressive (e.g. Kasha and Sequin-Swartz, 1983). There appears to be little impediment to the development of sporophytic morphology in the presence of the haploid nucleus.

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V. THE CAUSAL APPROACH TO ALTERNATION A. GENERAL ASSUMPTIONS

In interpreting the observational and experimental data described above it will be assumed that gametophytic and sporophytic morphology and behaviour are each determined by the integrated activation of a number of specific, but probably not contiguous, genes. It is further proposed that the form of growth will depend upon the balance of the activation, rather than one set of genes being completely repressed. Many genes, particularly those concerned with basic metabolism, are likely to be active in each phase. In Ulva, for example, no major differences could be detected between the soluble proteins from gametophytic and sporophytic plants (Hushovd et al., 1982). The differences so far detected in algae affect cell wall chemistry. In the red alga Gigartina, although carrageenan levels are of the same order in sporophyte and gametophyte, the sporophytic carrageenan is poorer in 3,6-anhydrogalactose, and richer in sulphate groups (Pickmere et al., 1973). In a number of siphonaceous algae a regular alternation in the chemistry of the cell wall is correlated with the different growth habits of the two reproductive phases (Tanner, 1981). In the flowering plant Tradescantia, Willing and Mascarenhas (1984) have concluded from an analysis of mRNAs from pollen and shoots that a large proportion of the genes are active in each phase. Similar discoveries have been made in respect of Zea mays (Willing et al., 1988; SariGorla et al., 1986) and Lycopersicon (Tanksley et al., 1981). It appears, therefore, that the number of genes concerned with the reproductive phase may be relatively few. After establishing the sites at which change of phase occurs, the causal approach to the problem of alternation becomes one of identifying the features likely to affect the balance of gene activity at those sites. B. FROM GAMETOFWYTE TO SPOROPHYTE IN THE LOWER PLANTS

1. The Uniqueness of the Female Gamete In looking for intimations of alternation in sexual cycles of algae and homosporous land plants, it seems reasonable to concentrate on the female gamete. There is no evidence that spermatogenesis in zooidogamous plants leads to a gametic cytoplasm rich in developmentally important molecules. The principal gene product appears to be tubulin (Schedlbauer et al., 1973; Pennell et al., 1988) destined for the motile apparatus. The main contribution of the male gamete to the zygote, apart from tubulin in the form of microtubules and axonemes, is a nucleus in which the chromatin is condensed or compacted, not a state associated with transcription.* It is doubtful whether the few organelles of male origin play a significant morphogenetic role. In Chlamydomonas the chloroplasts of the two mating strains fuse, but the * Note, however, the evidence recently presented for the presence of mRNA in the condensed nucleus of the spermatozoid of the fern Phyllitis scolopendrium (Rejon er al., 1988).

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DNA of one appears to be depolymerized (Sager, 1972; Nakamura et al., 1986). Little information is available from other algae. Although the fate of the “limosphere” (a plastid-mitochondrion complex appressed to the nucleus during differentiation of the spermatozoid in mosses (La1 and Bell, 1975)) is obscure, it seems unlikely that plastids are inherited from the male side in either bryophytes or pteridophytes. In the pteridophytes the few incoming male mitochondria are probably degraded in the zygote (Myles, 1978; Sheffield and Bell, 1987). The situation elsewhere is unknown. The development of the copious cytoplasm characteristic of the female gamete is initiated in both algae and archegoniates by one or more unequal divisions. Although the control of unequal divisions is obscure, once the inequality is established, the separate development of the larger cell, which retains most of the cytoplasm, is assured. Further plasmatic growth, accompanied by enlargement of the nucleus and decondensation of its chromatin, leads ultimately to the distinctive ultrastructural features of the mature gamete. So similar are these features in algae and archegoniates that it can be tentatively assumed that the cytochemical features, currently known principally from the ferns, are also similar. It seems likely, for example, that transcription and translation accompanying oogenesis (Fig. 2) will be found to be general, and also possibly transcription unaccompanied by translation continuing into the mature gamete (Fig. 2). The discovery in ferns that if thiouracil is introduced into this RNA. the egg cell, following fertilization with a normal spermatozoid, will give rise to an embryo tending to revert to gametophytic growth (Jayasekera and Bell, 1972), is a clear indication that at least part of the transcription is concerned with the change of phase. The concept of the mature egg cell being already programmed for sporophytic growth seems well founded. Of less evident morphogenetic significance are the aggregates of granular material present in the nucleus and cytoplasm of mature egg cells of algae, bryophytes and ferns, probably in all instances consisting, as in the ferns, of acidic protein. Since this material appears at a time when the chromatin is highly dispersed, it may represent a temporary sequestration of a protein or proteins concerned with chromosomal structure. Also of doubtful significance in relation to change of phase are the high levels of DNA in the mitochondria and plastids of fern eggs, again possibly a feature of egg cells of other lower plants. Besides permitting rapid replication of these organelles during embryogenesis, some of this DNA may be mobilized and utilized in the synthesis of nuclear DNA. Evidence for this is that in the presence of tritiated thymidine the first divisions in the embryo remain unlabelled (Bell, 1961). More relevant to alternation may be the indications in high-resolution autoradiographs of cytoplasmic DNA not satisfactorily related to mitochondria or plastids (Sigee and Bell, 1971). This may correspond to the cytoplasmic I-somes, small packets of informational DNA, believed by E. Bell

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(1969) to be present in differentiating animal cells and to play a role in controlling protein synthesis. The relatively high level of basic proteins in the cytoplasm of egg cells (as detected by the Sakagouchi reaction) raises the possibility of this DNA being in the form of a chromatin-like complex (Bell, 1963). These considerations lead to the view that in the lower plants the balance of gene activity shifts in favour of sporophytic growth during oogenesis. The causes of this shift are probably to be sought in the progressively richer plasmatic environment in which the nucleus in the female lineage finds itself. Throughout oogenesis the cell with the larger complement of cytoplasm appears to act as a powerful sink, attracting to itself an increasing share of metabolites. Its sister cells remain depauperate or even diminish. In the archegonium the demands of the egg cell appear to be such that the organization of the other cells in the canal cannot be maintained. They suffer lysis in consequence. At the time of maturation, the boundary of the canal is conspicuously thickened and the chamber sealed. It seems likely, therefore, that the products of lysis, amongst which will be nucleotides and polypeptides, are retained in the canal. The egg cell in its final phase of maturation will thus be brought into intimate contact with a concentration of complex molecules, some or all of which may be taken into the cytoplasm. Among prokaryotes the genome is known to respond readily to changes in levels of essential nutrients, and gene activation is adjusted accordingly (see Gottesman (1984) for review). There is no evident reason why eukaryotes should lack comparable regulatory networks. The finalization of the shift in the balance of gene activation towards the sporophytic phase can reasonably be regarded as the response of the genome of the egg cell to the enriched environment of the archegonium. The final size of the female gamete appears to bear little relationship to change of phase. The significance of the very large egg cells of the cycads, for example, is probably to be sought in the general biology of the group. The concept of the uniqueness of the female gamete is supported by the results of fusing gametophytic protoplasts. In mosses this results in a parasexual hybrid of gametophytic form and function (Grimsley et al., 1977). A closer approach to normal fertilization was achieved in Grifithsia with the fusion of protoplasts from male and female plants. The resulting growth did not, however, take on a sporophytic function. 2. The Signijicance of Apogamy Parthenogenesis. In view of the foregoing arguments it might be expected that the parthenogenetic development of female gametes would not be uncommon. This appears to be so in the Chlorophyta (Ettl et al., 1967), although it is not always clear that the development is truly sporophytic. Certainly in Ulva, which has an isomorphous cycle, the sporophytic nature of the thalli arising from unfertilized gametes is confirmed by the attempted meiosis

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in the zoosporangia (Tanner, 1981). The situation in the brown alga Ectocarpus siliculosus is similar (Miiller, 1967). Nevertheless, more detailed information is required on the cytology and cytochemistry of oogenesis in the algae before the hypothesis can be effectively assessed. Surprisingly, in the homosporous archegoniates, parthenogenesis, although reported, has not been conclusively established. In the instance of Ampelopteris prolijer, in which parthenogenesis was claimed following treatment of cultures with IAA (Mehra and Sulklyan, 1976), it was not clearly demonstrated that the sporophyte originated from an egg cell. The old account of Athyriumfilix-femina var. clarissima Bolton clearly needs checking if the variety can be rediscovered. Despite many attempts, von Wettstein (1924) was unable to stimulate partially extracted unfertilized egg cells of either the haploid or diploid races of the moss Funaria hygrometrica into growth of any kind, although adjacent cells regenerated protonema. La1 ( 1 984) reports parthenogenesis in cultures of Physcomitrium. Although these results are impressive, the growth of the moss in vitro was markedly slower than in nature, and fertilization did not occur when the cultures were flooded. It is conceivable that oogenesis in the cultures was imperfect, and the cell which gave rise to the sporogonium not comparable with a normal egg. The reluctance of the unfertilized egg cell in both bryophytes and pteridophytes to develop further may be a consequence of the dispersed state of its chromatin. The compact chromatin of the male nucleus possibly provides a template facilitating the reassembly of the chromosomes and the entry of the zygotic nucleus into mitosis. Natural apogamous cycles. The apogamous cycles of many ferns can be reconciled with the notion of cytoplasmic enrichment, possibly coupled in some instances with the additional influence of a hybrid nucleus. The omission of cell division accompanying the formation of the restitution nucleus, events which seem to depend on a failure of tubulin synthesis at this time, results in the mother cell entering meiosis with a substantially greater,amount of cytoplasm than the corresponding cell in a sexual relative. The richer endowment of cytoplasm is subsequently reflected in the larger spores. The conditions for a shift towards effective sporophytic activation are therefore set, but not completely. A brief gametophytic phase is still necessary. The cytoplasm of gametophytes is envisaged as becoming more elaborate in successive cell generations. Normally this leads to archegonial initials, but in the apogamous ferns to the sporophytic outgrowth. Many, but possibly not all (Gastony, 1985), apogamous ferns are believed to be of hybrid origin (Manton, 1950). Heterozygosity in the genome may stimulate gene activity, leading, in the presence of the favoured cytoplasm, to a relatively rapid transition to the sporophytic phase. There is a parellel with the apogamy induced in allotetraploid species of Dryopteris (Manton and Walker, 1954) by preventing sexual congress. Here, however, the hybrid nucleus is interacting with

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cytoplasm derived from a normal spore and the transition takes correspondingly longer.

Induced apogamy and chromosome number. Although clearly defined instances of apogamy (apart from parthenogenesis) are wanting in the algae, the many examples in mosses under cultural conditions suggest that the balance in gene activity in these plants can be readily shifted. Increased richness of the medium is usually an effective factor. In the instance of sporogonia produced directly from protonema, unequal divisions yielding small cells with dense cytoplasm are a conspicuous intermediary feature. In ferns, except for the allotetraploids mentioned above, the transition to sporophytic growth is less readily achieved, but it is promoted in a similar manner. It has long been evident that chromosome number itself does not determine form, but in the lower plants it is not without its effects. In algae, for example, parthenogenesis in Cladophora (Foyn, 1934) appears to follow a doubling of the chromosome number at some stage preceding oogenesis. In the bryophytes and ferns, diploid races tend to apogamy (but not parthenogenesis) more freely than haploid. Particularly responsive species may be allotetraploids (Lazarenko et al., 1961; Manton and Walker, 1954). Pteridium, reluctantly apogamous, appears from electrophoretic studies to be genetically diploid (Wolf et al., 1987), and the gametophyte correspondingly haploid. The absence of any clear boundary separating the gametophyte and sporophyte in both natural and induced apogamy indicates the lack of antagonism between the contiguous tissues. This contrasts sharply with the situation in sexual reproduction. The continuity of the cells is an indication of the nearsporophytic condition of the gametophytic cells at the site of the transition. C. FROM SPOROPHYTE TO GAMETOPHYTE

1. Sporogenesis and Microsporogenesis: the Irrelevance of Meiosis The congruence of meiosis and change of phase in the natural cycle immediately suggests a causal relationship. The extensive changes often observed in the cytoplasm at this time have been interpreted as indicating a “clean up” of the cytoplasm (Dickinson and Heslop Harrison, 1977), providing a tabula rasa upon which the transcription and translation relating to the gametophytic phase can proceed uncontaminated by information persisting from the parent sporophyte. Two arguments can be advanced against this interpretation. First, although the events in Lilium (upon which the views of Dickinson and Heslop Harrison are largely based) are indeed spectacular, they are not universal. Change of phase may occur without any significant loss of ribosomes. Second, the notion that the effective expression of the gametophytic genes calls for a new set of ribosomes is difficult to sustain. Although ribosomes

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vary in composition, there is no evidence that a particular composition is associated with a particular kind of growth. The ribosome appears to be purely a functional unit. A more plausible interpretation of the events in Lilium is that they are related to the needs of the meiotic nucleus. The thickened boundary of the mother cell probably prevents the ingress of all but simple nutrients (Heslop Harrison and Mackenzie, 1967), but meiosis, following on the previous mitosis and of short duration, calls for a rapid synthesis of DNA and (for the synaptonemal complexes) of RNA. The essentials are provided by the depolymerization of nucleic acids in the cytoplasm. A parellel is provided by the depolymerization of chloroplast and cytoplasmic ribosomes during spermatogenesis induced by nitrogen starvation in Chlamydomonas. The nucleotides so mobilized are utilized in the replication of the chromosomal DNA preceding the mitosis yielding the gametes (Siersma and Chiang, 1971). In the meiotic system it is possible that ribonucleotides also play a role in promoting the pairing of the homologous chromosomes. Mehra and Kumari (1986), for example, present remarkable pictures of pseudo-meioses in root tips of Ptrrotheca,falconeri in the presence of a range of ribonucleotides. Since there are only three pairs of chromosomes in the species, and the karyotype is readily recognizable, there is no doubt that in many instances tetrads of four haploid nuclei were produced in the meristematic region in response to the treatment. In species in which no significant ribosome depolymerization occurs during meiotic prophase, the needs of the nucleus are presumably met by anabolism of the simple nutrients able to enter the mother cell. This is likely to be relatively protracted and lead to a lengthy prophase.

2. The Significance of Apospory in the Lower Plants That meiosis is not essential for change of phase is unequivocally demonstrated by aposporous regeneration in lower plants. Indeed, in Oedogonium apospory is clearly an alternative to meiosis in the same cell, leading in either instance to gametophytic growth. Although aposporous regenerates may show gigas characters, they are unambiguously gametophytic in form and reproductive behaviour. The gametes are normal and functional, but the development of the embryo, particularly in ferns, may be retarded and irregular. Until other evidence becomes available, it can be tentatively assumed that, as in the fern Pteridium, there are no cytological phenomena in aposporously regenerating cells resembling those seen in meiotic prophase in the same plant. The essential conditions for apospory in the bryophytes and ferns (the algae and fern allies have not yet been adequately studied) can be tentatively identified as the isolation of a portion of the sporophyte, by excision o r otherwise, from the correlating influences of the whole plant and its subjection to nutritional stress (Sheffield and Bell, 1987). Experiments with the fern

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Todea show that even zygotes develop in a prothalloid manner when isolated and subjected to these conditions (DeMaggio, 1963). The reluctance of successively more mature tissues to yield gametophytic regenerates must indicate some kind of stability acquired as the sporophyte becomes established and possibly implanted in the proteins of its cells. This would make it increasingly difficult to shift the balance of gene activity towards the gametophytic by experimental means.

3. A UniJiedTheory of Sporogenesis The inadequacy of hypotheses associated with meiosis to account for the alternation in the form of growth characteristic of sporogenesis promotes the search for other features of sporangia likely to be significant. In land plants, sporangia tend to be isolated organs, terminating the tips of slender axes or filamentous stalks. In the sporangium the spore mother cells are surrounded by thickened walls of restricted permeability (to judge from the micrographs, also a feature of sporogenesis in the alga Dasya). The boundary of the tapetum is often thickened and in some instances reinforced by an acetolysisresistant membrane. These features can all be reasonably regarded as effecting the isolation of the sporogenous cells from the correlating influences of the parent plant, and also a restriction of their nutrition to simple molecules. They provide a striking parallel to those that bring about aposporous development in experimental conditions. Both sporogenesis and aposporous systems can be envisaged as generating a form of cytoplasmic impoverishment. This is the precise converse, for example, of the situation in the archegonium, and the balance in gene activation is correspondingly reversed towards the gametophytic. The metabolic stress imposed in the sporangium may need to be particularly severe, since the cells concerned are derived from mature tissue. The evidence from lower land plants generally supports the interpretation of sporogenesis advanced here. Microsporogenesis is so similar in all its essentials that it seems highly likely that the same arguments apply. Unfortunately knowledge of sporogenesis in the algae is too limited to allow a reasoned assessment. The shift in gene activation having been achieved, and the immature spores released from the tetrad, transcription can proceed (Franks and Mascarenhas, 1980; Raghaven, 1985). The physical activity at the surface of the nucleus noted earlier is probably related to the establishment of the gametophytic phase. The significance of the “nucleoloids” often present in the cytoplasm is obscure. If RNA is found to be absent, they may be similar to the aggregates of acidic protein occurring in the cytoplasm of fern eggs. 4 . Megasporogenesis The special features of megasporogenesis. Except for Isoetes (and possibly Stylites) and those flowering plants in which all four megaspores enter into

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the formation of the embryo-sac (as in Lilium), megasporogenesis involves the degeneration and lysis of other cells in the sporogenous lineage. Other than in Selaginella, the degeneration is normally restricted to meiotic products. The causes of degeneration are obscure. In Marsilea it has been argued that the degeneration of three spores in each tetrad has a Mendelian basis (Bell. 1979), and there is evidence that this may also hold for flowering plants (Bell, 1979; Correns, 1900). Other explanations call upon gradients within the tetrad and pressure fields within the ovule (see Pennell and Bell (1987a) for discussion). Whatever the causes of degeneration, the surviving megaspore comes to enjoy an environment enriched by the products of lysis. From a causal point of view this is likely to be the most significant feature of megasporogenesis. The causul aspects of megasporogenesis. The lytic products which bathe the maturing megaspore are unlikely to be without effect. In Myosurus, for example, representative of species with monosporic embryo-sacs, the situation of the surviving megaspore strikingly resembles that of the egg cell in a fern (Fig. 5). Taxus presents a similar picture (Pennell and Bell, 1987a). There is no a priori reason why confinement in an enriched environment should not affect the maturing spore and egg cell in exactly the same way. If this interpretation is correct, the predominance of the gametophytic genes, established in the young spore by the conditions of sporogenesis already discussed, will be rapidly reversed as the megaspore matures. Evidence for this view is that in flowering plants, callose, characteristic of the interface of gametophyte and sporophyte, begins to disappear from the wall of the tetrad as the viable megaspore is formed (Rodkiewicz, 1970). The apparent exceptions to this reasoning noted in the preceding section are worthy of further attention. Spore production in Zsoetes resembles that in Platyzoma, differences in spore size being related to differences in the number of spore mother cells. It is therefore conceivable that extended culture of megagametophytes of Zsoetes (in this instance heterotrophic) might, in the absence of fertilization, lead to the production of antheridia. This would indicate that the tendency towards oogenesis and the initiation of sporophytic development were not firmly established. In Lilium, according to Rodkiewicz (1970), the wall of the megaspore mother cell lacks callose at any stage. During meiosis the cytoplasm accumulates paracrystalline arrays of protein (Dickinson and Potter, 1978), possibly utilized in the organization of the tetrasporic embryo-sac. The cytology suggests that after an initial isolation the boundary becomes sufficiently permeable to permit the inflow of nutrients. Active syntheses would then provide an environment within the developing sac tipping the balance of gene activation once again in the direction of the sporophytic. Despite the cytological and cytochemical parallels between the maturation of the egg cells of homosporous archegoniates and the surviving megaspores

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\

Fig. 5. Diagrlim to show the physiological similarity between the situations of (left) the maturing egg cell of a fern (e.g. P/rridiuni) and (right) the maturing megaspore of a flowering plant (e.g. M w \ uru.s),

of heterosporous plants, the nucleus of the mature megaspore (unlike that of the egg cell of a homosporous plant) remains capable of division. The comparative readiness with which parthenogenesis can be induced in heterosporous ferns and flowering plants, and sporophytic outgrowths obtained from megagametophytes of gymnosperms, indicates that the lineage derived from the megaspore retains its incipient sporophytic state. The haploid conifer Thuja gigantea var. gracilis (Pohlheim, 1968) also presumably arose parthenogenetically, or directly from the megagametophyte. Further evidence in support of the view that the megagametophyte is already becoming sporophytic is the simplicity of the archegonium in the heterosporous archegoniates. Less nucleus+ytoplasm interaction would be required to complete the activation of the sporophytic genes in the gamete. The sporophytic condition imposed during megasporogenesis appears to be particularly stable. Fragments of sporophytes, single cells and protoplasts, if they regenerate at all, yield sporophytic tissue, either directly or by way of callus. There are no reports of regeneration yielding pollen tubes or embryosacs. Apospory in flowering plants bears little resemblance to that in homosporous archegoniates. Aposporous embryo-sacs contain egg cells which invariably develop parthenogenetically, in sharp contrast to the equivalent situation in mosses and ferns. If Cortaderia jubata (Philipson, 1978, and personal communication) is representative, the boundaries of aposporous em-

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bryo-sacs bear no callose. It seems likely that, although resembling normal embryo-sacs, they are effectively sporophytic, lacking any interaction leading to a callosed interface with the nucellar tissue in which they arise, and from which the embryo freely draws its nutrition.

VI. GENERAL CONCLUSION As interpreted in the foregoing, the two reproductive phases in the life cycle of the photoautotrophs depend upon an alternating enrichment (oogenesis) and subsequent deprivation (sporogenesis) of the cytoplasm. This in turn alters the balance of the expression of the relevant genes, and the form of growth and reproduction is determined accordingly. The essentials of the cycle are seen most clearly in the Pteridophyta, and the sites of change of gametophyte to sporophyte and sporophyte to gametophyte are readilyh identifiable and separated by independent somatic development. In experimental conditions the balance in gene activity can be more readily tipped towards the gametophytic than the sporophytic. Nevertheless, the combined effects of gene dosage and hybridity increase the readiness with which the balance can be tipped from the gametophytic to the sporophytic, as evidenced by the polyhaploid gametophytes of allopolyploid species of Dryopteris and Pteris. Gene expression can be made altogether more labile by mutations, as evidenced by horticultural varieties of ferns such as those of Athyrium and Phyllitis (Andersson-Kotto, 1938). Apogamous cycles in ferns can be satisfactorily related to the general hypothesis. Indications from the algae (the relevant information is still fragmentary) are that the principles identified in the homosporous land plants will also apply here. The bryophytes also conform, but the balance in gene activity in mosses can be more readily tipped in either direction by experimental means than in any other homosporous land plants. Heterospory and megasporogenesis do, however, introduce a new situation. The gametophytic phase on the female side is contracted both morphologically and physiologically. Enrichment takes place in the maturation of the megaspore, and the balance of gene activity begins to tip in the direction of the sporophytic state before oogenesis. In addition, gametophytic gene activity in flowering plants appears to be particularly vulnerable, as evidenced by the comparative ease with which embryogenesis can be induced in pollen grains and unpollinated ovules. Tapetal activity, prominent in vascular plants (in the seed plants particularly on the male side), is probably not significant in relation to change of phase. Spores of ferns and fern allies (Pettitt, 1979a), and microspores of conifers (e.g. Taxus (Pennell and Bell, 1986)) and flowering plants (e.g. Lilium (Dickinson, 1970b)) are enveloped in a coat of their own making before becoming exposed to the tapetum. The coat may act as a molecular sieve and

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exclude informational molecules. Moreover, the tapetum is itself an isolated tissue (particularly where there is a peritapetal membrane), and its products may also be gametophytic. This would account, for example, for the ability of tryphine, the pollen coating of tapetal origin, to evoke the incompatibility response at the stigma surface in a plant such as Raphanus (Dickinson and Lewis, 1973). The “reaction body” formed in the wall of the stigmatic papilla at the point of contact is similar in form and composition to the thickened boundary which develops between gametophyte and sporophyte in archegoniate plants, and which in gymnosperms has been related to precipitation reactions between extracts of these tissues (Pettitt, 1979b). The principal significance of the tapetum probably lies in the production of sporopollenin, augmenting that produced by the spores themselves, and in the release by lysis of simple nutrients supporting their development. The current ability to locate particular molecules in cells at high resolution by means of immunogold cytochemistry will make it possible to detect the instant at which proteins characteristic of the incoming phase appear, or become augmented, at the sites of change. Alternation is not explained by discoveries of this kind, since its roots lie in the general development which leads to reproductive maturity. Nevertheless, the information does help to identify those aspects of development which are specifically concerned with change of phase, and hypotheses based upon these observations can to some extent be checked by experiment. The problem of alternation will probably be solved by concentration on species in which the phases are clearly defined, and other aspects of development are as uncomplicated as possible. The lower land plants and some algae meet these criteria, and await investigation by the powerful techniques now available.

ACKOWLEDGEMENT The author acknowledges with much appreciation profitable discussions of various aspects of this paper with colleagues in many places.

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The Formation and Interpretation of Plant Fossil Assemblages

ROBERT A . SPICER

Department of Earth Sciences. Oxford University. Parks Road. Oxford OX1 3PR. UK

I . Introduction . . . . . . . . . . . . . . . . . . . . 96 A . The Quality of the Plant Fossil Record . . . . . . . . . . 98 B. Vegetational Heterogeneity . . . . . . . . . . . . . 100 I1 . Plant Remains as Sedimentary Particles . . . . . . . . . . . 101 A . Allochthonous and Autochthonous Assemblages . . . . . 101 B. Settling Velocity . . . . . . . . . . . . . . . . 103 111. AerialDispersalandTransport ofplant Organs . . . . . . . 104 A . Leaf Abscission . . . . . . . . . . . . . . . . 104 B. Organ Dispersal by Wind . . . . . . . . . . . . . 106 IV. Litter Degradation on the Forest Floor . . . . V. Aquatic Processing of Plant Debris . . . . . A Initial Processes-Floating . . . . . . B. Transport in the Water Column . . . . . C . Leaf Degradation . . . . . . . . . VI . Fluvial Transport . . . . . . . . . . . A . Channel Deposits . . . . . . . . . VII . Lacustrine Environments . . . . . . . . . A . Fluvio-lacustrine Deltas . . . . . . . VIII . Fluvio-marine Deltas and Estuaries . . . . . A . Pro-delta Slope . . . . . . . . . . B. Distributary Mouth Bars . . . . . . . C . TidalFlats . . . . . . . . . . . . D . Interdistributary Embayments . . . . . E. Beaches . . . . . . . . . . . . . F. Lower Delta Plain Marshes . . . . . . G. Upper Delta Plain Marshes . . . . . . H . DeltaicLacustrineand Fluvial Environments I . DetritalPeats . . . . . . . . . . . Advances in Botanical Research Vol . 16 ISBN 0-12-005916-9

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Peat and Coal Assemblages . . . . . . . . . . Vulcanism . . . . . . . . . . . . . . . A. The Importance of Explosive Vulcanism to the Plant Case Studies . . . . . . . . . . . . . B. DebrisFlow . . . . . . . . . . . . . C. Preservation in Air-fall Tephra . . . . . . . D. Lateral Lakes in Volcanic Terrains . . . . . . E. Post-eruption Vegetation Recovery. . . . . . Preservation and Diagenesis. . . . . . . . . . A. Compression/Impressions . . . . . . . . . B. Duripartic Preservation . . . . . . . . . C. Tissue Mineralization . . . . . . . . . . D. Casts and Moulds . . . . . . . . . . . .

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I. INTRODUCTION The study of the history of life on earth involves far more than describing the morphological details of fossils and documenting phylogenies. Every fossil represents evidence that an organism lived, not in isolation, but in the context of a physical setting populated by other organisms. In order to understand the history of life it is essential that the organisms represented by fossils are studied in their proper context; as part of a network of interacting physical and biological agencies that shape the lives of individuals and influence the contribution of those individuals to the processes and patterns of evolution. The environment in which an individual exists is determined not just by contemporaneous conditions, but also by physical and biological circumstances that have preceded it. The palaeontologist must therefore adopt a distinctly four-dimensional view of the world, spanning geological and biological disciplines. Terrestrial life forms of 100 million years before present (mybp) might seem exotic enough, with dinosaurs and coniferous mangroves, but at least we would find some familiarity in small mammals and flowering plants. But further back, in the Carboniferous coal forests of 300 mybp, or the middle Devonian heathlands of 380 mybp, landscapes, and possibly the atmosphere, were more alien. In these environments, plant and animal species, the communities of which they were a part, and the climates in which they existed, were quite unlike those of today. However, these organisms, and the ecosystems which shaped them and in which they lived out their lives, ultimately gave rise to our modern world. In

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a very real sense, if we wish to understand fully the structure and process of our present environment, and predict accurately the likely consequences of our actions on natural systems, then we have to understand the past. The fossil record provides invaluable data regarding the biotic effects of global climate changes (and in so doing charts those changes), the causes and consequences of wholesale extinctions, and outlines the course of organic evolution. However, the traditional approach of the palaeontologist, in which specimens tended to be investigated in isolation for their morphological or anatomical characteristics, can only provide a partial insight into ancient ecosystems. In recent years a major change in emphasis in palaeontology has been away from the study of individual isolated specimens. Instead a more integrated biological and geological framework is being developed. We are not only seeing the establishment of a more organismal approach, in which the remains are viewed in terms of once-living organisms, but by the analysis of populations of fragmented and less well preserved material in a sedimentological context, we are also gaining the ability to reconstruct, with the minimum of conjecture, whole ancient communities, ecosystems and climates. This approach, which promises to revolutionize our understanding of ancient environments, depends for its success on our ability to interpret correctly how such assemblages were formed and how they represent the source communities. The study of the processes of fossilization is known as tuphonomy. The term was introduced by the Russian palaeontologist Efremov (1940), who considered it as being “the study of the transition (in all its details) of organic remains from the biosphere into the lithosphere”. As such, taphonomy is a subject that encompasses aspects of anatomy, morphology, whole-organism biology, ecology, sedimentology, fluid dynamics, and both biochemistry and geochemistry. Taphonomists seek to identify and, ideally, to quantify, the various sampling biases inherent in transport, deposition and lithification processes that distort the image of ancient life that is discernible from the fossil record. Taphonomy is of fundamental importance in the accurate interpretation of individual fossil specimens or accumulations of remains. These accumulations, or assemblages, are usually not suites of the remains of whole organisms but represent fragmented parts, variously degraded, of a range of different individuals and species that lived at varying distances from their ultimate site of deposition and burial. The taphonomist seeks to understand the processes that gave rise to fossil assemblages and thereby reconstruct ancient communities and environments as accurately as possible. Most biologists accept that evolution has taken place and that within lineages morphologies change with time. Implicit in this acceptance is an appreciation that a changing morphology must often be associated with changing behaviour and tolerance of individual organisms to external conditions. It follows that the structure and composition of communities also’are subject to

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change. A limit exists, therefore, to the extent to which the present can be used to interpret the past. Biological organisms are not, in large part, timestable, and the principle of uniformitarianism (“the present is the key to the past”) can be applied to biological organisms only with extreme caution. To make palaeobiological interpretations as reliable as possible, and to avoid circularity of argument, taphonomic work, in the first instance, should emphasize the most time-stable assemblage formation processes. Mostly these processes are physical and chemical. Implicit in the broad scope of taphonomy is the requirement for an integrated multidisciplinary approach. The complexity of fossilization processes may be an important reason why taphonomy has only recently emerged as an identifiable and legitimate area of endeavour. Traditional compartmentalization of subject areas and specialization has tended to restrict serious taphonomic investigation, but since the early 1970s taphonomy has contributed greatly to our understanding of ancient life. Ideally plant and animal taphonomy should be reviewed together, because plant-animal interactions are an integral element in shaping ecosystems, the composition of fossil assemblages, and the pattern of evolution. An important aim of palaeobiology is to understand the interdependence of extinct animals and plants, and this can only be done with a strong taphonomic input. Although there are numerous similarities in the way that animals and plants enter the fossil record, there are also sufficient differences to justify their separate treatment. In this overview I will concentrate on advances in plant taphonomy, although similar advances are occurring in animal taphonomy. A. THE QUALITY OF THE PLANT FOSSIL RECORD

An important difference between plants and animals is the way they fragment prior to burial. Unlike the majority of animals, plants are composed of, and produce throughout their lifetime, an indeterminate number of organs that are shed into the environment. These organs have greatly differing potentials for transport, deposition and preservation. For example, huge numbers of extremely durable and easily dispersed spores or pollen may be produced, but floral structures are usually delicate, ephemeral structures, produced in much smaller quantities. Only one trunk is produced by a tree, but leaves are produced in large numbers. Woody trunks may be transported great distances and undergo several cycles of deposition and remobilization prior to final burial, whereas leaves are less easily reworked. The range of reworking potentials exhibited by plant organs introduces another variable known as time-averaging. This phenomenon has long been recognized in animal hard-part fossils such as bones or shells. The durability of these elements means that they may be deposited, exhumed possibly thousands or millions of years later, and redeposited, perhaps alongside the

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remains of recently dead organisms. Thus most assemblages are likely to be time-averaged samples. The delicate nature of many plant organs minimizes the likelihood of time averaging, or at least reduces the averaging effect to a temporal resolution of less than the average life of an individual. However, some plant parts, notably logs and the walls of pollen grains and spores, can be highly resistant to decay and reworking. Assemblages of these organs therefore may contain a significant time-averaged component which degrades community resolution. A detailed understanding of taphonomy and sedimentology is required to minimize the danger of misinterpretations. Whole plants are rarely found in the fossil record and, consequently, palaeobotanical systematics has to handle isolated organs (see Spicer and Thomas (1986) for a number of papers dealing with this topic). Many years may elapse between the first discovery of a particular plant part and the eventual reconstruction of the whole plant. In practice very few whole plants are, or can ever be, reconstructed, and yet it is whole plants that comprise communities. In spite of this problem, plant communities leave ample evidence of their existence and composition in the form of assemblages of isolated organs. In a very real sense, a plant fossil assemblage gives a biased measure of the capacity of the source vegetation to produce litter. Litter production in turn is related to biomass and productivity and as suchis governed by factors such as soil conditions, climate and exposure, community composition, and seasonality (Bray and Goreham, 1964; Bonnevie-Svendsenand Gjems, 1957; Krassilov, 1969; Spicer, 1981). The total amount of litter produced by a stand of vegetation varies from year to year as the community approaches equilibrium with the environment (the climax state), or is disturbed by disease, fire, flooding, grazing etc., or interannual climate fluctuations. A given fossil deposit may be the result of a sudden event such as a flash flood or a volcanic eruption, and therefore it may sample plant debris produced predominantly within a single year. Less catastrophic depositional events reflect the gradual accumulation of material over periods of time sometimes lasting as long as several millions of years. It is therefore extremely difficult to relate directly the quantity of organic material in an assemblage to any similar measure of the source vegetation. Very crude estimates of regional productivity may be made (for example, large coal reserves point to high net accumulation rates of plant debris, and thereby a high ratio of organic productivity in relation to organic degradation or inorganic sediment input), but these estimates are not appropriate for single assemblage analysis. The reasons for this will, I hope, become clear in the course of this chapter. Before proceeding, however, the term “assemblage” will be clarified. A plant fossil assemblage is an accumulation of plant parts, derived from one or several individuals, that is entombed within a volume of sediment that is laid down under essentially the same conditions. This definition allows for

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the differentiation of assemblages on sedimentological or biological grounds. The best resolution available in the fossil record for community reconstruction is determined by the smallest sedimentological unit that can be recognized that contains a statistically valid sample of the source community. Previously I have proposed that, for quantitative sampling, the concept of the sedimentation unit of Otto (1938) should be employed (Spicer, 1981), and this concept is included in the assemblage definition. In writing this overview of what is a rapidly expanding, yet infant, field of endeavour, I have attempted to present our current state of knowledge and the principles upon which it is based, rather than give an exhaustive review. I have chosen to concentrate on the taphonomy of megafossils (leaves, fruits/ seeds, logs etc.) rather than microfossils (spores/pollen), or molecular fossils (e.g. see Runnegar and Schopf, 1988). I have adopted this approach because a comprehensive introduction to one aspect of plant taphonomy is more likely to be coherent and useful than a superficial treatment of a wider range of topics. B. VEGETATIONAL HETEROGENEITY

Plant species are not uniformly distributed in space or time. In ecological work it is convenient to categorize the heterogeneity within vegetation in terms of communities, and often these blocks of coexisting interacting individuals are labelled in terms of characteristic component taxa. For any given set of more or less constant conditions, sera1 development leads to the establishment of a stable community that is in equilibrium with its environment. The temporary stages involved in the development of this “climax” community usually follow a recognizable sequence or track in which a succession of taxa come and go until the climax state is reached. Ecotonal gradients between adjacent communities in both time and space can also be recognized. This view of plant interaction is one that is useful to the palaeoecologist because resolution of source vegetation at the level of spatial relationships between individuals is difficult to achieve (but techniques and understanding are improving), whereas resolution at the level of community blocks is possible in many instances. Just as communities are not stable on an ecological time-scale, in geological time their composition and character changes with changing environmental (particularly climatic) and evolutionary conditions. Just as the individual lineage evolves, so too does community composition and identity. It is therefore highly misleading and dangerous to extrapolate too far back in time from modern ecosystems. We must think in terms of evolutionary ecotones as well as spatial ecotones, and rely on the fossil record to provide insights into communities and their interactions for which there may be no modern analogues. Fossil assemblages form when plant debris is buried by sediment suffi-

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ciently rapidly to limit or prevent biodegradation. Because the movement of sediment is involved, the sites of potential fossil formation are dynamic ones where old land surfaces, and the vegetation they support, are being destroyed, and new subaerial land surfaces are being formed and colonized. The communities that act as sources for potential fossil assemblages are in a state of flux to a greater or lesser degree. Debris from disturbed vegetation is more likely to enter the fossil record than climax communities, and yet there is often an implicit assumption in plant palaeoecology, and in particular its application to palaeoclimatology, that the ancient vegetation being studied was in equilibrium with its environment and that the assemblage is an unbiased sample of that source. Nothing could be further from the truth; but that does not mean to say that the fossil record cannot be used for palaeoecological or palaeoclimatological reconstructions. Plant fossil assemblages are highly complex data banks that demand skilled interpretation. The complexity is, at first sight, daunting, but, provided the patterns of assemblage formation are understood, the fossil record is capable of yielding considerably more information about ancient ecosystems than is presently generally appreciated. As an example of the mosaic of communities and seral stages that can be sampled by a river system, consider Figs 1 and 2. Meandering of the hypothetical river erodes into mature “climax” forest of the floodplain. Whole trees, forest litter, and understorey and ground vegetation may fall into the river by bank erosion, while litter may be blown onto the water directly by wind. On the opposite bank, the inside of the bend, sediment is being deposited and being colonized by plants. Litter from communities reoresenting several seral stages may be blown into the river. Similar erosional and depositional processes with attendant differences in vegetation occur on upstream and downstream ends of islands. Further downsteam levee banks, being several metres higher than the surrounding floodplain, are better drained and support a more diverse community than the backswamps and interfluves. However, levee litter is rarely preserved on site because the soils are well oxygenated. The situation is not as negative as it appears. If taphonomic processes are understood, and the fossil assemblage is sampled in such a way as to reveal taphonomically important data, fossil assemblages allow the reconstruction of ancient communities in spatial and temporal relationship to each other. Indeed, it is only through the fossil record that the evolution of communities can be studied.

11. PLANT REMAINS AS SEDIMENTARY PARTICLES A. ALLOCHTHONOUS A N D AUTOCHTHONOUS ASSEMBLAGES

A plant bequeaths evidence of its existence to the fossil record either by

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Fig. I. Block diagram illustrating fluvial depositional environments. a, channel lag deposits with logs (see Fig. 14); a'. abandoned channel lag deposits; b, point-bar seres; b', upper point-bar deposits entombing litter derived from upstream riparian sources and local point-bar communities; c. levee communities and deposits; d, undercutting of river banks introducing whole trees and forest floor litter representing mature interfluve communities; e, abandoned channel infill deposits (see Fig. 2).

Fig. 2. Diagram of a vertical section through an active channel normal to flow at meander bend. a, undercutting by high flow velocities at the outside of the bend introducing whole trees and litter from interfluve communities; b, channel lag deposit composed of coarsest channel sediment and logs primarily derived from undercut banks upstream; c, channel lag deposits buried by laterally accreting point-bar deposits-erosion at a and deposition at c causes the channel to migrate laterally, in this case from left to right; d, deposition of plant and inorganic sediment with hydrodynamic settling properties intermediate between those of material found at e and b; e, deposition in upper point-bar sequence of comparatively fine-grained inorganic sediment and plant litter derived from upstream sources and local communities; f, litter from various point-bar sera1communities.

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naturally abscising various organs that are subsequently transported to a site of sediment accumulation or by becoming buried in situ. Assemblages that are the result of the accumulation of transported material are termed allochthonous assemblages, whereas those that represent accumulation in situ are termed autochthonous. With the exception of peat and coal accumulation or catastrophic inundation, both of which give rise to autochthonous assemblages and will be dealt with later, most plant fossil assemblages are the result of the accumulation of detached organs that have undergone some degree of transport from the site of growth to the site of burial. The interaction of plant parts with sedimentary processes, to produce either autochthonous or allochthonous assemblages, has been termed hiostratinomy (Gastaldo, 1987a). Although the transport potential of different plant organs varies enormously, two basic factors are important: the fluid dynamic properties of the organ, and the position of its point of release into transport media (usually air or water). The way a detached plant organ (or organ fragment) interacts with a fluid medium is potentially governed by the density of the plant particle in relation to that of the fluid medium, together with its shape, size and surface characteristics. B. SETTLING VELOCITY

Let us, for the moment, consider a leaf about to be abscised from the crown of a tree. The “flight” characteristics of that leaf will determine how far the leaf will travel in any given wind speed before it reaches the ground. The further the leaf can travel, the greater the chance it has of encountering a depositional environment. Genetic and environmental factors determine the shape, size, and surface characteristics of the leaf, but density will in part be dependent on the moisture content of the leaf. Sedimentologists have long been able to describe, in approximate terms, the fall of inorganic (usually quartz) grains by treating them as spheres. Many equations in fluid dynamics require that the particle under consideration be ascribed an effective geometrical dimension. For a sphere this dimension is the diameter and, of course, remains the same irrespective of the orientation of the particle to the fluid flow. For a two-dimensional object such as a leaf, such a simple dimension is difficult to ascribe, because as the leaf falls, its orientation is likely to change. Lateral oscillations, or other manifestations of instability during fall, are produced by the formation of a turbulent wake behind the falling object. The generation of this wake can be predicted by calculating a dimensionless number, the Reynolds number, which is proportional to the ratio between inertial and viscous forces. The Reynolds number is given by

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where U is the fall velocity, L is the effective dimension, p is the density of the particle, and ,u is the dynamic viscosity of the fluid. At low Reynolds numbers, fluid flow past the particle is laminar and the particle descends in a stable orientation. Such conditions exist when the particle is extremely light or the fluid very viscous. At higher Reynolds numbers, however, a turbulent wake is generated which imparts instability to the falling object. To overcome the problem of assigning a single length dimension when the orientation of the particle is constantly changing during fall, various measures that combine dimensions such as length and width have been used (e.g. Allen, 1984; Clift et al., 1978). None are entirely satisfactory and the difficulties in predicting fall behaviour on theoretical grounds have forced a more empirical approach (e.g. Ferguson, 1985; Spicer, 1981).

111. AERIAL DISPERSAL AND TRANSPORT OF PLANT ORGANS The first stage in the formation of fossil assemblages composed of detritus from plants growing in subaerial environments is the shedding of plant parts, either by natural abscission or trauma, into air. Bias introduced into plant assemblages by the timing and frequency of shedding and selective wind transport can be, and usually is, profound. Aerial transport determines what sample of organs a river or lake, for example, receives, and therefore the image of the surrounding vegetation “seen” by the body of water. Many plant organs such as spores, pollen grains, fruits and seeds have become specially adapted to enhance their transportability by wind for reproductive purposes. Intuitively one might expect these organs to be well dispersed by wind and thus have an increased probability of encountering a depositional environment. Other plant parts behave very differently. For example, in the normal course of events floral structures develop into fruits and seeds, and any parts that are shed (e.g. petals) tend to be delicate “throw away” structures with little preservation potential. The leaves of herbaceous taxa are not even shed naturally, and instead wither, rot or fragment, still attached to the parent plant, and thus are most unlikely to enter a deposit except, perhaps, when overwhelmed by event sedimentation (e.g. floods, volcanic ash falls). Between these extremes lie the majority of plant organs. Because of their abundance and utility in biostratigraphy and palaeoclimatic studies, leaves of woody angiosperms have received most attention regarding their relative propensity for wind transport (Spicer, 1975; Roth and Dilcher, 1978; Ferguson, 1985). A.

LEAF ABSCISSION

Marked seasonality is associated with synchronous leaf fall (deciduousness).

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In modern temperate environments, leaf fall is most noticeable in the autumn, where leaf loss limits frost damage or water stress when the soil is frozen. This phenomenon is most marked in woody angiosperms because broad, thin leaves render them susceptible to freezing and desiccation. Most needle-leaved and microphyllous conifers, with small leaf surface area to volume ratios, and thick epicuticular waxes that limit water loss, are able to withstand these conditions. Some broad-leaved angiosperm taxa (e.g. Rhododendron, Ilex, Hedera) also thrive in understorey situations but these, like the conifers, have thick cuticles and surface waxes. In the case of evergreen taxa, and to some extent deciduous taxa, leaf fall is not restricted to the autumn but occurs year round. Evergreen leaf abscission does not occur at a constant rate, however, and may peak in response to the spring growth spurt or in response to temporary drought. Temperate evergeen leaves tend to remain functional on the parent plant longer than tropical evergreen counterparts (often as little as seven months (Longman and Jernik, 1974) and therefore comparable to temperate deciduous species) and consequently are likely to be under-represented in the fossil record (Ferguson, 1985). In tropical regimes, leaf abscission is also related to seasonality, and in particular the onset of dry conditions. Deciduousness here is often facultative in response to severity of drought, but in some cases the rhythm has become endogenous (Ebel et al., 1985). Ferguson (1985) cites Janzen (1975) as saying that in deciduous tropical forests many woody riparian plants do not experience synchronous leaf loss, but renew their leaves continuously. Continuous leaf loss in rainforests is interpreted as a means of ridding the plant of epiphyllous growths, insect infestation (Ferguson, 1985), toxic metabolic wastes, or to ensure a continuous recycling of nutrients. Leaf abscission can also be induced by changes in daylength and low light levels. Many shade leaves are abscised when they no longer receive sufficient light to “break even” on food production versus respiratory requirements. In the past, forests are known to have flourished under polar regimes where they apparently experienced winter darkness lasting several months (Spicer and Parrish, 1986; Spicer, 1987). Here synchronous leaf abscission was probably triggered primarily as a response to photoperiod rather than to the occurrence of frost. Evergreen plants can similarly be induced to shed leaves synchronously as a response to “shading” by heavy surface deposits of volcanic ash (Burnham and Spicer, 1986). The amount and frequency of litter supply to potential depositional sites affects greatly the preservation potential of the material. Where leaf fall is continuous (i.e. lack of seasonality), the activity of biotic degrading agents can become attuned to litter supply (Hynes, 1961) and, characteristically, little material survives to enter the fossil record. The general low level of forest litter in the tropics is well known. Even in temperate regimes the life cycles of aquatic organisms may become

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synchronized with autumnal litter input (Hynes, 1961), which acts as a primary food energy source (Egglishaw, 1964; Cummins et al., 1972, 1973). Indeed, it is most likely that ever since they appeared, the activity of detritivores has been linked with food supply. Furthermore, the most constant and reliable food source (typically riparian plants for reasons I shall outline later) have been those most “preferred” by detritivores. As a result many common taxa local to depositional environments have long been subject to preferential loss from the fossil record. Spicer (1981) reports an example where Alnus, the most common tree surrounding a temperate lake, was rarely represented by leaves in the lake sediments (except where sedimentation rates were high), whereas leaves from trees in surrounding slope vegetation (e.g. Fugus) were common in lake-bottom debris. Clearly this has considerable palaeobotanical implications. On the other hand, massive synchronous leaf loss may temporarily overwhelm the detritivores, permitting leaves, particularly those locally derived, to enter a sedimentary environment and form a concentration of organic material of the kind likely to attract the attention of palaeobotanists. This is particularly true if leaf fall is accompanied by seasonal highs in rainfall, run-off, and sediment deposition. 6. ORGAN DISPERSAL BY WIND

I. Factors Aflecting Fall Velocity in Still Air The time taken for a plant organ to fall a measured distance in still air is a basic property that determines the relative transportability by wind. The longer an organ takes to fall, the further it can be blown. The behaviour of leaves as they fall is a critical factor affecting fall velocity, and it would be extremely valuable to be able to predict fall behaviour from leaf morphology alone, because morphology is often all that survives in the fossil record. In a series of laboratory and field experiments, Ferguson (1985) studied the “flight” properties, ground dispersal, and degradation of a variety of leaves of temperate woody species, and to date this represents the most comprehensive study of these aspects of taphonomy. Leaf weight. Weight per unit area at abscission is the most critical intrinsic property of a leaf that affects flight and ground dispersal. All other factors being equal (which usually they are not), a light leaf will be blown further than a heavy leaf in any given wind speed. Typical fall rates for leaves of different weights per unit area are shown in Fig. 3. Ferguson investigated the abscission weight of a number of evergreen and deciduous taxa. For the 49 taxa studied, leaves weighed between 0.0057 and 0.072 g cm-2, with the higher values belonging to evergreens. The leaves of some taxa (e.g. Fugus sylvaticu, Quercus robur) potentially weigh very little at abscission. This is because these plants retain their leaves long after leaf senescence so that the leaf desiccates before it falls. This contrasts strongly

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with taxa that abscise leaves while they are still green and moist (e.g. Alnus glutinosa and Salix nigra). In natural systems the effective weight per unit area of a leaf is governed by prevailing atmospheric conditions. Wet leaves will be heavy. The relative importance of this factor remains to be quantified. Leaf shape. Ferguson and Spicer carried out fall experiments using paper and natural leaves (Spicer, 1981; Ferguson, 1985) (Fig. 3) and found that leaf weight per unit area was the attribute most strongly correlated with fall time in still air. More recently, however, Ferguson (1985) has reported that shapes with major axes of markedly different length (long and narrow) tend to rotate about the longer axis; this behaviour slightly increases fall time and therefore the chance of greater dispersion from the source. Leaf size. Although leaf size does not appear to be obviously correlated with fall rate in still air, size is important with regard to movement through the branch and trunk space within a forest. Large leaves will tend to encounter static obstacles more frequently than small leaves, and any such event will either trap the leaf directly, or cause the leaf to plummet towards the ground. Ferguson (1985) noted a weak positive correlation between leaf size and

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weight per unit area. Such a correlation would tend to favour the transport of smaller leaves. However, although 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 is a function of their exposure to high wind energies and their initial height from the ground (Spicer, 1981). Petiole efects. Although the petiole only exceeds 20% of total leaf weight in a small number of cases, in some taxa (e.g. Acer pseudoplatanus) it can be substantial and one might expect that large petioles would affect significantly the flight properties of those leaves that possess them. Preliminary experiments (Ferguson and Spicer, unpublished data) indicate that removal of petioles from Plutunus x hispanica leaves has an insignificant effect on fall rate. Compound leaves. Ferguson (1985) has made some interesting observations regarding leaflet abscission in compound leaves. In Aesculus hippocastunum, whole or nearly whole compound leaves may be shed, whereas in other taxa leaflets may fall indiscriminately. Such patterns of abscission will affect the relative proportions of leaflets in an assemblage, and, if mistaken for whole leaves, could significantly bias palaeoclimatic and floristic interpretations. Some taxa typically retain the terminal leaflet (e.g. Juglans regiu), whereas others shed all the leaflets before abscising the main leaf stalk (e.g. Robinia pseudoacacia). To date there appears to be no general distinction in the pattern of leaflet loss between palmate and pinnately compound leaves. Ferguson (1985) points out that in units that are shed with only a few leaflets remaining, the weight of stalk ensures that they fall close to the parent tree, thus limiting their chances of entering the fossil record. The frequent occurrence of such leaves in a fossil deposit would indicate a very local source.

2. Dispersion Resulting from Air Full Ferguson (1985) observed that forest floor litter is usually spatially very heterogeneous, and the composition a t any one site reflects strongly the trees in the immediate vicinity. Dunwiddie (1987) cites C. Grier as showing that 90% of conifer needles fall within a 20” cone projected from the tip of the parent tree. This limited dispersal can be partly explained in a closed canopy forest by the fact that wind energies in the intertrunk space are generally low. However, several workers have shown that aerial dispersal of leaves away from a source follows a negative exponential model (Szczepanski, 1965; Richerson et ul., 1970; Edmonds and Benninghoff, 1973; Rau, 1976; Spicer, 1981). The form of the equation used by Rau (1976), who studied litter deposition in an open lake, is: 2, = 2, exp ( - k[r - x])

where x = distance from the lake centre, 2, = deposition occurring at distance x , r = distance from the lake centre to the shoreline, Z,= deposition at

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the shoreline, and k = (r - x ) - l In ( Z J - l ) . Figure 4 illustrates the relationship. This form of the equation, under ideal circumstances of well-defined lake margins and known inorganic sedimentation rates could allow estimates of ancient litter productivity to be obtained from the fossil record. In any kind of vegetation, even the modest dispersal suggested by the negative exponential model for open sites is likely to be greatly curtailed by low wind energies and physical obstruction. From studies based on actual observation, Ferguson (1985) suggests that horizontal dispersal during air fall rarely exceeds a distance equivalent to the height of release, and therefore is likely to exceed the height of the source tree only in exceptional circumstances.

3. Post-descent Dispersal Over Land Surfaces Leaves blown along the ground are distributed laterally by a combination of

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saltation and rolling. In laboratory experiments, in which a variety of flat paper leaf shapes were blown over a smooth flat surface using a fan, the greatest dispersion was found with circular shapes that tended to roll (data of Ferguson and Spicer, published in Spicer (1981)). Folding the shapes to form a “V” when viewed along the fold axis increased dispersion, but imbrication introduced a marked skewness to the shape of the histogram. Dry, curled leaves will thus be transported further than wet leaves, which also will tend to stick together. Dispersal was little affected by leaf size but, as with fall velocities, weight per unit area did prove important, with light leaves travelling the furthest (Fig. 5). The question remains, however, as to how important these differences are in natural situations. Ferguson (1985) noted that in planted, single-species forest plots, little mixing of leaf litter occurs between plots. To investigate the extent of ground transport he placed a pile of 500 dry Fugus sylvutica leaves in a coppice of A h u s glutinosa. After 98 days only one leaf had travelled more than two metres. In open herbaceous landscapes, however, similar experiments showed greater dispersal because not only are wind energies higher, but many leaves temporarily come to rest supported above the ground on the herbaceous layer, thus allowing wind to get under the leaves and suspend them in the turbulent moving air column. Ferguson concludes that most woodland leaves are rarely disseminated very far from the parent trees and that even the tallest temperate trees must be growing within 50 m of a body of a water in order to stand any chance of their leaves becoming fossilized. Although there are exceptions, in general this statement is true and has major implications regarding the interpretation and reconstruction of ancient vegetation. Storm Effects In the foregoing I have concentrated on what might be described as “normal” wind transport. In many lower latitude areas today, and in the past, high wind energies associated with storms and hurricanes are common events that can shape communities and influence the fossil record. The most obvious effect of storm action is to introduce large quantities of fresh plant macrodetritus into sedimentary environments by traumatic removal of above-ground plant parts (Craighead and Gilbert, 1962; Scheihing, 1980; Dittus, 1985). Canopy trees and emergent crowns are those exposed to the strongest winds and likely to suffer the most damage. Material derived from these sources is also likely to be transported the furthest and to be incorporated rapidly into the potential fossil record by the high sedimentation rates that often accompany storms. However, damage to these forest components may subsequently result in increased biomass production by the surviving subcanopy components and lead to a temporary change in community structure. 4.

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Hurricane-force winds, though not common, do occur in middle latitudes and their effect with regard to the fossil record is likely to be extremely variable, depending on the nature of the vegetation and the disposition to leaf abscission. A useful example here is provided by the effects of the October 1987 storms in southern England. In spite of the autumnal predisposition towards leaf fall, the high winds (> 160 km h- l ) failed to strip deciduous trees of their leaves. As a consequence, many mature trees were uprooted or suffered breakage of the trunk or major branches. Had the leaves been more easily shed, trauma would have been less severe because of the reduced wind resistance offered by naked branches (cf. volcanic eruption effects). The day after the storm I observed the River Medway nearing bank-full

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discharge transporting numerous leaf-bearing branches. Isolated floating leaves were not as numerous as one might have expected. Fallen trees (e.g. Fugus, Quercus, Populus, Tiliu) retained their leaves for several weeks, and leaves remaining on upright deciduous trees were blackened and desiccated, and in some cases tattered, but again remained on the trees for several weeks. From these observations one might postulate that sedimentary deposits resulting from this storm would have a limited flora, but had the storm occurred a few weeks later, when more leaves would have been shed or more easily stripped from the trees, leaf accumulation would have been considerably greater. It follows from this that storm damage to predominantly evergreen vegetation is likely to be routinely marked by a high proportion of broken branches and trunks and forest damage. The quality of leaf, fruit and seed assemblages formed under these conditions is difficult to predict, and more work is clearly needed on this aspect of plant taphonomy. In temperate regimes with mostly deciduous vegetation, storm damage effects will be strongly dependent on the timing of the storm in relation to foliar condition. Several fossil assemblages have been specifically ascribed to storm (wind) effects (e.g. Potonie, 1910; Wnuk and Pfefferkorn 1987). The usual criterion for recognizing such deposits is directional tree blow-down in the absence of fluvial or volcanic sediments that could provide alternative explanations for log orientation.

IV. LITTER DEGRADATION ON THE FOREST FLOOR In an earlier publication (Spicer, 1981) I implied that mechanical degradation of dry leaves in subaerial environments was likely to be minimal. Although in general this remains true, Ferguson (1985) reported the results of experiments which show that this need not be the case. Ferguson tumbled a selection of dry leaflets of Aesculus hippocustanum for a period of 2 weeks in a 20-cm diameter drum at 100 rev min-*. The result of this somewhat harsh treatment was the attrition of intervascular tissue until mostly only the primary and secondary veins remained. Dry leaves tend to be rigid and brittle and thus predisposed to collision breakage. They also tend to be curled, which enhances their transportability by wind. In most circumstances litter will be moist at the time of abscission or become wet soon after landing on the forest floor. High moisture content tends to render leaves flexible and as a result they tend to lie flat on the substrate and suffer less lateral wind transport. If the surfaces of the leaves are wet they will tend to stick to each other and to the substrate. Moisture also predisposes the leaves to bacterial and fungal degradation, particularly if precipitation leaches out water-soluble polyphenols that tend to inhibit decay. According to Ferguson (1989, the composition of the saprotrophic community, and therefore decay rate, is determined by climate, the nature of the

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1 13

Fig. 6. Diagrammatic section through a gallery forest bordering a river showing principal sources of litter (stippled) sampled by the river. The forest on the left is shown supporting a dense growth of climbers that dilute the litter contribution from forest trees. (Modified from Ferguson. 1985.)

substrate, and the composition of the litter. To this one must add the geological time period because evolutionary development of the community is also likely to play a significant role. Decay on the forest floor is highly selective. Experiments with mixed species of leaves in nylon mesh bags (Ferguson, 1985) showed that while some species (e.g. Fagus sylvatica, Platanus x hispanica) suffered little decay after I5 months, other taxa (e.g. Acer pseudoplatanus, Alnus gfutinosa) were skeletonized. Ferguson suggests that the overall composition of the litter will affect which elements are selectively lost in that litter that is primarily composed of resistant species, moderately resistant taxa will be preferentially destroyed. On the other hand, in a situation where easily degraded taxa predominate, the moderately susceptible species preferentially survive. Similarly, the degradation sequence will be determined to a large extent by litter composition. In some circumstances these differences in decay rates may be linked to specific vegetational components. For example, in Puerto Rican montane rainforest, litter decay is faster in principal successional taxa forming the uppercanopy than in secondary taxa (La Caro and Rudd, 1985). Once a plant organ is incorporated into forest-floor litter, its capacity for entry into an aquatic sedimentary environment is reduced greatly. Some material is blown laterally into stream systems and lakes (Fisher and Likens, 1973), but as discussed above, this contribution is small if the vegetation is closed, although it may be more significant in more open environments (Ferguson, 1985). Vegetation bordering open water, where the forest canopy is broken, tends to be rather dense (Richards, 1966), presumably due in large part to increased light levels. This creates a wall of riparian vegetation often specialized with a high proportion of climbers, which not only filters out litter produced by (and more representative of) the forest as a whole, but also contributes large quantities of debris of its own (Fig. 6). Undercutting of river banks by channel migration or bank-full discharge

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leads to direct input of forest-floor litter, much of which is likely to be partly degraded and partly water saturated. In many instances live herbaceous ground cover is also introduced into river systems (Figs 7 and 8). The introduction of such material to sedimentary environments enriches greatly the potential fossil assemblage, not only in terms of the quantity of organic debris but also in terms of organ and species richness (Spicer, 1980; Spicer and Wolfe, 1987). Indeed, many organs that do not normally enter allochthonous assemblages (e.g. roots and heavy seeds/fruits or branches and that have a limited capacity for lateral dispersal) may be represented. However, the mixing of litter from one location with that from another, the selective degradation processes that operate on the forest floor, and the mixing of forest-floor litter with relatively fresh material, are all likely to generate an assemblage that can only be regarded as a bulk sample of vegetation within the drainage basin as a whole (Spicer and Wolfe, 1987). Bank erosion is also responsible for the frequent introduction into river systems of whole living trees (Fig. 8a). When this occurs, leaves and most branches are stripped from the trunks, which may sink to the river bed and be deposited as part of a basal lag or stranded on banks or bars. Typically the flared root systems survive abrasion enough to encounter the river substrate. The still floating log then swings around in the flow so that the upper part of the trunk points downstream (Fig. 8b). The absorptive capacity of root systems persists after death, so that logs with roots attached tend to sink root end first (Greer, unpublished data). This not only contributes to “root stranding” but can give rise to apparent “in situ” forests with transported trees in life position provided that water depth is great enough and flow is virtually non-existent. This phenomenon has been noted in lakes surrounding Mount Saint Helens, where many trees were snapped by volcanic blast several feet above ground level before being blown or washed into the lakes (Coffin, 1983). In contrast, bank collapse seldom results in snapping or preferential rotting of the trunk a short distance above the root system. Instead, long lengths of trunk survive. The ratio of trunk length to root base diameter of these logs dictate that their most stable configuration is horizontal. The discovery of upright tree bases in non-volcaniclastic sediments suggests strongly that the trees have been preserved at their site of growth by inundation of the forest by sediment. In volcanic terrains the situation is very different and will be discussed in detail later.

V. AQUATIC PROCESSING OF PLANT DEBRIS The entry into an aquatic environment brings about profound changes in material derived from terrestrial sources. The following discussion will be based on the assumption that the material under consideration has been dir-

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Fig. 7. (a) Aerial view of floodplain depositional complexes showing both active and abandoned channels (Yukon River floodplain, central Alaska); (b) bank collapse introducing trees from mature floodplain communities; (c) community heterogeneity on successive floodplain accretionary surfaces.

ectly transported to the water surface by wind. Similar processes operate on detritus that has been in the forest-floor environment before entering the aquatic realm, but partial saturation, leaching, and decay processes will have already taken place to a greater or lesser extent. A.

INITIAL PROCESSES-FLOATING

Immediately upon landing on the surface of a body of water, plant material,

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Fig. 8. (a) Detail of active bank erosion exposing interfiuve vegetation in vertical cross section from which litter derived from all forest strata can enter the river (Yukon River, central Alaska); (b) bar-stranded whole trees alligned parallel to flow with root balls facing upstream, flow is from right to left (Yukon River, Alaska).

e.g. a leaf, begins to absorb water and soluble substances begin to be leached out. Initially a dry leaf will float and may remain buoyed up by surface tension for considerable periods of time (more than several weeks), provided only that the bottom surface of the leaf is wetted and the water surface is calm (Spicer, 1981). Conceivably, plant material could be transported long distances this way, but such conditions are only likely to pertain in slowflowing rivers protected from wind (i.e. subcanopy streams). These are situ-

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EXPLANATION No agitation of surface water

h

Frequent agitation of surface water

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ations in which long-distance transport is unlikely to occur because of small stream size. The uptake of water by leaf tissues is governed by cuticle and epicuticular wax thickness, abundance of stomata and/or hydathodes, damage to the lamina or petiole and water temperature and chemistry (in particular oxygenation (Spicer, 1981; Ferguson and De Bock, 1983; Ferguson, 1985)). Leaf anatomy may also be important (Ferguson, 1985; Greer, unpublished data). In view of these variables, and incomplete preservation in fossils that only rarely allows quantification, several workers have set out to establish ranges of floating times in order to evaluate the likely role of differential floating in assemblage formation. Typically, experiments have been conducted in aquaria with moderate frequent agitation to simulate wave action. Spicer (1981), Ferguson and De Bock (1983) and Ferguson (1985) have all noted that floating times range from several hours to several weeks, with thin chartaceous (papery) leaves tending to sink first, and thick coriaceous (leathery) leaves floating the longest (Figs 9, 10 and 11). Because individual leaves within a population exhibit a range of floating times that follows an “S”-shaped curve, the most useful statistic for comparing floating times is the “half-life” (Ferguson, 1985). Present results suggest that lamina damage (holes) and petiole loss both decrease floating times. According to Ferguson (1985), the leaf stalk of compound leaves acts in much the same way as petioles on simple leaves in that it takes longer to saturate and buoys up the leaf. Thus intact compound leaves float longer than their individual leaflets. The floating times of dispersed fruits and seeds (diaspores) have also been investigated from the view of both reproductive dispersal (Praeger, 1913; Ridley, 1930) and taphonomy (Collinson, 1983). In general, diaspores exhibit

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a greater range of floating times than do leaves. Floating times do not appear to be related directly to diaspore size because small seeds can remain afloat for several weeks. Floating times seem unrelated to the habit of the parent plant (Collinson, 1983). Wood and, in particular, logs can remain afloat for several years (Spicer, personal observation; Coffin, 1983), and potentially, therefore, the only hindrance to log dispersal throughout a drainage system downstream from the growing point is water (channel) depth and instream obstacles. In particular, where ancient channel deposits suggest water depth was adequate for log transport, and yet no large logs are found in spite of an abundance of other

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plant remains, there is a real possibility that large trees were absent from the community. The long floating times of logs also raise important questions regarding the use of fossil tree rings for climate interpretation when the trees in question are preserved in marine sediments. Today the western end of the Alaskan Peninsula is treeless and yet the beaches are littered with thousands of drifted logs. These trees are derived in large part from the area of Japan and therefore carry an allochthonous climate signal. Although floating transport of plant debris is obviously an important factor in mixing material derived from different source communities, all the while a plant organ is protruding from the surface of the water or lies in the surface waters it is also subject to the effects of wind. In this way material can be moved across a lake (often several times) before sinking, and rivertransported material may be blown to the sides of the channel where it may become stranded. B. TRANSPORT IN THE WATER COLUMN

Once the specific gravity of any object in fresh water exceeds unity, that object will sink. In most plant material this condition is achieved by progressive water absorption. Progressive 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 the condition of full saturation is reached. When and where the object eventually settles is determined to a large degree by submerged density and shape: two factors that are important in determining settling velocity and entrainment behaviour. When submerged, an object may be moved while being suspended by turbulence in the water column or by rolling and bouncing (saltation), or by gliding along the stream bed. The length of time a plant organ is transported in these modes depends largely on its settling velocity and the rates of water flow. Settling velocity also determines to a large extent the depth distribution of suspended solid materials in the water column. In general this distribution is logarithmic, but the complex interaction of the planar shapes of many plant parts with the turbulent eddies present in most natural flow regimes prevents the detailed modelling of this distribution for organic debris. Nevertheless, a knowledge of the relative magnitudes of plant organ settling velocities is necessary to assess relative sorting potential. 1 . Settling (Fall) Velocity in Water Settling velocity of fully saturated plant organs has been investigated experimentally (Spicer and Greer, 1986; Greer, unpublished thesis) using a 2 x 2 x

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2 m settling tank. In spite of their irregular two-dimensional shapes, angiosperm leaves exhibit a surprising degree of within-taxon uniformity of settling velocities, as do more prismatic shapes of conifer needles (Fig. 12). Even very irregularly shaped material, such as isolated fern pinnules and moss leafy shoots, have fall velocities that fall within narrow, moderately welldefined limits (Fig. 12). Statistically, no significant difference exists between the fall velocities of different broad-leaved taxa (including Ginkgo and fern pinnules), but significant differences do exist between conifer needles and broad-leaved taxa, and among individual conifer taxa (Greer, unpublished thesis). On the basis of these results one might expect no substantial hydraulic sorting to occur among angiosperm taxa, where sorting would be related strongly to settling velocity (e.g. in a flow velocity gradient over a fluvio-lacustrine delta slope). On the other hand, leaves of conifers are likely to be separately deposited from angiosperm leaves derived from the same community: a phenomenon that has been observed in the field (Spicer and Wolfe, 1987). In general, conifer needles have higher settling velocities (e.g. 3.03 cm s-' for Piceapungens at full saturation) than angiosperm leaves (e.g. 1.5 cm s - ' for Fagus sylvatica at full saturation), although individual leaves of other broad-lamina taxa such as Ginkgo biloba sometimes exhibit fall velocities as high as 6.7 cm s when petiole and lamina configuration produce a hydrodynamically efficient shape that results in a stable gliding fall. The extension of these studies to diaspores and fragmented leaf material would prove most valuable. 2. Entrainment and Burial For any given flow rate, particles concentrated near the stream bed will be

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mostly those with the greatest settling velocities. The heaviest particles will be transported as bedload and be in suspension only for brief periods of time. As current flow wanes, the lighter fractions will progressively settle out. Conversely, increases in current flow progressively entrain material. Flow rate in natural streams and rivers is rarely constant and plant debris is likely to undergo several cycles of deposition and entrainment before permanent burial takes place. Deposition and entrainment of plant particles is a complex and as yet poorly understood process. For less variable, flakey inorganic particles such as mica, experimental results have been ambiguous (Schoklitsch, 1914; Shields, 1936; Pang, 1939; Mantz, 1973, 1977; Berthois, 1962), even though plane sedimentary beds (defined as plane to within one solid particle diameter) were used. Leaf orientation and aspect in relation to fluid flow will clearly determine the flow velocity at which entrainment will take place. Curved leaves or planar particles that are inclined with their raised edge facing into the flow will be picked up at lower flow rates than those that are flat on the stream bed or inclined with their raised edge pointing downstream. Indeed, inclination at this latter orientation will result in higher stream velocities merely pressing the object more firmly onto the stream bed until turbulent eddies disrupt the particle, or scour around the particle allows flow to occur beneath it. Bed roughness clearly plays a major role in particle entrainment. By means of flume experiments, Greer (Greer, unpublished thesis; Spicer and Greer, 1986) has been able to show that not only bed particles but also bedforms play an important part in entrainment sorting. If the bedforms (e.g. ripples) were large enough for the particles to settle in the troughs, they were protected from entrainment and often buried rapidly by bedform migration. Larger particles were cleanly swept through the system. Thus, for example, 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. By means of flume experiments, Rex (1985) investigated the burial of selected plant debris in simulated stream flow. Migration of bedforms was the main mechanism of stem burial but this played only a partial role in hollow stem infilling. Rex found that sediment in suspension entered prostrate hollow stems as steep-fronted wedges infilling from both open ends even when the stem was aligned parallel to flow. The degree of infilling was dependent on the dimensions of the hollow void, and in particular the diameter of the void in relation to its length. Rarely did long, narrow stems fill completely, because closure of the open ends by sediment prevented sediment penetration to the midsection of the stem length. By means of dye experiments with glass tubes, Rex (1985) showed that the process of infilling was governed by flow separation and vortex generation induced by restriction of flow as the fluid passed over and through the stem tube. Tubes with one end

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closed (caused, for example, by stem nodal diaphragms, crushing, or abutment to bedforms) reduced infilling further, and blocked tubes never completely filled under the conditions operating in the flume. In Rex’s (1985) experiments, sediment transported as bedload filled stems orientated parallel to flow in a somewhat different fashion, in that the infilling sediment wedges had a less steep leading edge, and showed a distinct graded structure favouring the deposition of the coarser sediment fractions. Infilling of stems oriented with their long axis not parallel to flow was similar to that seen with suspended sediment, but the structure and degree of infilling was not as constant and depended on stem orientation and length. Comparisons with fossil stem fills (Rex, 1985) showed that this approach was valid and provides a potential method of determining the sedimentological regime during burial. However, as Rex (1985) points out, the incomplete filling of tubes with a closed end poses real problems in the interpretation of completely infilled fossils such as the stigmarian root systems seen in the Fossil Grove, Victoria Park, Glasgow (cf. MacGregor and Walton, 1948). Gastaldo et al. (1987) observed that flooding of lowlands is not usually accompanied by a leading “wave” of water, but occurs by raising of the water table. The resulting gradual inundation saturates most of the plant litter before flow rates become strong enough to transport the organics. As water flow increases to peak flood stage, transported inorganic sediment is trapped by the still. in situ saturated mat of forest-floor litter. This actually enhances sedimentation rates and thus burial of the plant litter. Similar processes probably takes place on organic-rich channel bottoms and may be responsible for the incorporation of leaf beds into the sedimentary package (Gastaldo et al., 1987).

C. LEAF DEGRADATION

I . Biological Most leaves entering an aquatic environment become decayed or damaged before they are deposited. Immediately upon entering the water, soluble compounds such as sugars, various mobile elements (e.g. potassium) and some polyphenols (decay-limiting compounds) begin to leach out, and within days leaves reach equilibrium with the chemistry of the surrounding water (Nykvist, 1962; Spicer, 1975). If the polyphenols are in the condensed or insoluble form, their antifungal and antibacterial properties can delay microbiological degradation (Bennoit et al., 1968; Williams, 1963). Leaves most susceptible to microbiological decay are those that have low lignin content, no or few condensed polyphenols, and a high sugar content at abscission (e.g. Alnus). Fungi and bacteria typically enter a leaf through stomata, lamina damage, or the petiole, and preferentially attack the internal tissues of the leaf. Fungi appear to be more important in leaf decay (Kaushik and Hynes,

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Fig. 13. (a) Typical patterns of leaf degradation caused by large particle invertebrate feeders; (b) typical patterns of leaf degradation caused by mechanical abrasion; (c) typical patterns of leaf degradation caused by microbial degradation.

1971). Where the cuticle is thick, all that may remain is an intact bag of cuticle (Spicer, 1981). However, the cuticle is not immune to breakdown, and when this occurs attack typically begins with the surface originally in contact with the epidermal walls, and the cutin of the anticlinal walls is the first to be degraded (De Vries et al., 1967). In leaves with thin cuticles, the cuticle tends to pull away in strips, and, because the spongy mesophyll is less resistant to degradation than the palisade tissue, the lower cuticle is often lost first (Ferguson, 1985). Colonization of the leaf tissues by fungi and bacteria also preferentially predisposes the leaf to attack by invertebrates (Kaushik, 1969; Petersen and Cummins, 1974). The type of degradation caused by invertebrates may be classified into that produced by large-particle feeders (rounded holes and arcuate damage to lamina margins) and small-particle feeders (removal of intercostal tissue and leaf skeletonization) (Fig. 13a,c) (Yonge, 1928; Petersen and Cummins, 1974). As with forest-floor degradation, the species mix will determine the extent to which any particular species is attacked, but in an aquatic system food sources other than terrestrially derived litter may be available. The presence of aquatic plants, and macrophytes in particular, greatly affects the benthic fauna by oxygenating the water and providing food and shelter (Rau, 1976; Ferguson, 1985). If alternative food supplies are available, invertebrates may not degrade leaf litter to any great extent (Webster and Waide, 1982; Dane11 and Anderson, 1982). Trophic state was considered by Ferguson ( 1 985) to be an important factor in selective leaf degradation. Ferguson postulated that in oligotrophic lakes, the generally low nutrient status would force micro-organisms to seek out leaf material, which in turn would lead to destruction by invertebrates. Leaf species rich in nutrients would be preferentially degraded. In eutrophic systems, however, the general availability of nutrients would lead to less species-selectivedegradation, although there is some evidence for enhanced leaf degradation in the presence of high nitrogen and phosphate availability

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(Hanlon, 1982; Newbold et al., 1983; Mathews and Kawalczewski, 1969; Kaushik and Hynes, 1971). Ferguson (1 985) also considered briefly the effect of temperature on leaf degradation and underscored the long-held assumption that decay proceeds more rapidly under warm, rather than cool, aerobic conditions. Invertebrate abundance is adversely affected by high sedimentation rates (Webster and Waide, 1982), and in unstable (i.e. rapidly fluctuating) regimes frequent disturbance is likely to keep population levels low. High sedimentation rates also lead to rapid burial of plant debris (and therefore isolation from invertebrate attack) and, particularly if the sediment is fine-grained, the development of anaerobic conditions. Oxygen depletion around the organic material is essential to preservation because this slows and eventually stops the decay processes. 2. Mechanical Degradation Waning water flows will commonly result in intervals of rapid sedimentation. Intuitively one might think that high energy flow regimes would degrade most plant material, but experiments using tumbling barrels (Ferguson, 1971, 1985; Spicer, 1981 ) show that even comparatively delicate plant organs such as leaves are remarkably robust when freshly abscised. However, leaves that have suffered even the slightest amount of microbiological attack are weakened substantially (Spicer, 198 1). The degree of mechanical fragmentation that takes place for any given flow regime and instream obstacle density is a function of the decay state of the leaf and its structure. These two factors are, of course, related and, as we have seen, decay is a function of a variety of environmental factors. The robustness of fresh leaves has been used as one line of evidence for the existence of wholesale deciduousness in Cretaceous near-polar forests. Spicer and Parrish (1986) examined a wide range of sedimentary facies in Late Cretaceous rocks on the North Slope of Alaska. In all sediment types, even fluvial sandstones, none of the leaf material exhibited significant biological or mechanical degradation. This was interpreted to mean that all the plant material was incorporated more or less simultaneously while fresh, and therefore as evidence of synchronous leaf fall (Spicer, 1987). Mechanical fragmentation is characterized by angular breaks and tears in the lamina and is quite distinct from damage brought about by biological agents alone (Fig. 13b). The presence of such damage in fossil leaves is strong evidence that they have undergone stream transport, and in favourable circumstances degradation studies may be used to differentiate growth sites. Such a situation might be the deposition of mechanically degraded, streamtransported leaves in a lacustrine setting where local taxa have suffered only biologically induced damage. Mechanical degradation of diaspores with hard protective coats is usually slow to occur (Collinson, 1978) and diaspores are, in general, more robust

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than leaves. Here again biological degradation is critically important and may well be the main agency for diaspore destruction (Collinson, 1983).

VI. FLUVIAL TRANSPORT River systems provide the route by which most larger plant organs may travel the greatest distance from the growth site. The size of the drainage basin and the volume and speed of water moving through the system will determine the maximum distance that any given plant particle may travel, but in reality this potential is seldom realized. The headwaters of a river are usually in areas of moderate to extreme topographic relief. This topography provides a wealth of edaphic and climatic environments in which vegetation of considerable heterogeneity can exist. Communities specific to certain altitudes or aspects can coexist within short distances of one another, and contribute litter to streams flowing past them (e.g. Spicer and Wolfe, 1987). The detritus from these distinct sources is mixed during fluvial transport over relatively short distances, and any resulting deposit provides a summary sample of the communities growing within the drainage basin (Spicer and Wolfe, 1987). Not all the communities are equally represented, however. Intermittent stream flow at the periphery of drainage basins exposes plant debris to wetting and drying cycles, stranding and entrapment on rough stream beds that quickly degrade even the most robust of plant material. Even where streams are permanent, high-velocity flow over rough substrates can impede transport. Greer, in Spicer and Greer (1986), reported the results of leaf transport experiments carried out in the devastated posteruption blast area of Mount Saint Helens (Washington, USA). In these experiments 1000 fully saturated and 1000 air-dried leaves of Fugus sylvuticu were released into a small stream system 1.2 km from its termination in a fluvio-lacustrine delta. The maximum flow velocity of the stream was 1.1 m s - l (corresponding to the narrowest-2.8 m wide-part of the channel), and the minimum velocity was 0.52 m s C 1 (channel width 15.5 m). The deepest part of the channel was 0.35 m at its narrowest point. Even under these ideal conditions, with no riparian or aquatic vegetation, only 0.2% of the unsaturated leaves, and none of the saturated leaves, reached the delta within 48 h after release. Entrapment occurred by stranding on the stream margins (mostly unsaturated leaves) or by imbrication against stream-bed obstacles (mostly saturated levels). In this instance, stream-bed obstacles consisted entirely of cobbles or gravel. In a normal vegetated environment, stems and branches would pose additional obstacles. Over time, the median point of each population moved downstream, indicating that many leaves were trapped in a metastable configuration, and could have been flushed further along the stream with increases in flow rate, but the time taken for any appreciable

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transport to occur exceeded that at which biodegradation substantially weakened the tissues and rendered them susceptible to mechanical break-up. The main factor in limiting downstream transport appears to be water depth and stream-bottom roughness in relation to the size of the plant particle. Small, high-energy streams occur in areas of greatest relief where depositional environments are generally considered rare. Tributary systems are erosive and a long way from depositional environments. The exceptions are intermontane basins in which plant remains are preserved in lacustrine sediments. Typically a valley may become dammed by a landslide or volcanic activity (lava or debris flow), resulting in the formation of a lake. Stream flow contributes inorganic sediment, and plant material and delta complexes result that reflect strongly the slope communities. The nature and value of these deposits will be discussed later. Although the potential for long-distance transport of meaningful samples of hinterland vegetation is severely limited in small, high-energy tributary systems, the situation is somewhat different in larger fluvial regimes (Ozaki, 1969). Several types of river have been recognized based on their generalized geometry (Allen, 1965, 1978; Bridge, 1984; Miall, 1982; Smith, 1983; Schumm, 1981). Braided rivers tend to form where discharge is highly variable and sediment load is often high (e.g. in glacial and seasonally arid environments), whereas highly sinuous (meandering) rivers are seen in lowenergy situations where flow and sediment load fluctuate little (floodplains with little seasonal variation in water supply). Topographic gradient, sediment supply, bedrock characteristics (in erosive settings) and climate are key elements in determining river channel course. These factors, and river geometry, determine the types of depositional subenvironments (channels, etc.) associated with the fluvial regime, and hence the quality of the plant fossil record in relation to the source vegetation. A. CHANNEL DEPOSITS

Water flowing along a natural channel does not move at a uniform rate. Frictional forces along the channel bed cause the water in contact with the channel boundaries to flow more slowly, and a vertical section through a channel, parallel to the axis of Bow, normally reveals a logarithmic distribution of flow velocities. Instability in the flow regime and natural obstacles cause river channels to become sinuous or to anastomose. Furthermore, whenever water flows around a curve, water on the inside of the bend flows more slowly than that on the outside of the curve. These differences in flow velocity lead to deposition and winnowing of sediments in different parts of the channel. Lag deposits form on the channel bottom (Figs 1 , 2 and 14) and are mostly composed of coarser material with the highest settling velocities. This material comprises the largest clasts that were being transported as part of the bed-

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Fig. 14. Hypothetical vertical section through an infilled abandoned channel. a, basal channel lag deposit containing logs from channel margins especially where channel sinuosity has resulted in bank erosion; b, early phase of infill during waning current-litter derived from riparian sources; c-e, successive infilling at repeated flood stages-litter derived from riparian, levee, overbank, and local “ox-bow” margin communities; f, final phase of infill as mire community develops organic-rich clay3 and peat to cap deposit-lateral and vertical changes in peat composition record the development of the mire community.

load, and lies on an erosional surface cutting into the underlying sediments. In a typical river channel with a broad-spectrum sediment supply, a lag deposit would consist of gravels or pebbles in perhaps a coarse sand matrix. Organic sediment would be made up of logs and larger, more robust, fruits and seeds. Occasionally, reworked clay balls containing more delicate plant parts may form part of a channel lag, but in such a case the material in the clay matrix may not have been contemporaneous with that in the rest of the channel sediments. Lag deposits are normally reworked as flow in the channel fluctuates, but they become preserved when the channel migrates laterally or is abandoned. Point-bars are typically (though not exclusively) formed in meandering rivers and are composed of sediments deposited by the slow-flowing water on the inside of channel bends. In many instances they bury and preserve the channel lag. Characteristically, point-bar sediments become finer grained upwards, have lateral accretion surfaces dipping down to the base of the channel, and possess a variety of bedforms, such as ripples, that decrease in scale upwards. The upper portions of point-bars are deposited in water with the least energy and typically contain the most diverse plant remains. Probably the best sample of riparian vegetation is to be found in these deposits, because robust material such as fruits and seeds and coriaceous leaves, as well as delicate elements such as flowers and even seedlings, can be incorporated. As with other depositional environments, the degree to which such material is preserved depends on the activity of the channel (as it affects subsequent erosion and deposition), and the colonization of the point-bar by later riparian vegetation. There can be little doubt that lag and point-bar deposits primarily sample riparian vegetation. However, the degree to which plant remains have undergone long-distance down-river transport before burial is more problematic.

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ROBERT A SPICER

Wide. often deep, channels provide ;I large water surface area and volume for the plant material to move in without becoming trapped by ohst* ‘ i-1~ e so r abraded and fragmented. I n quiet, slow-moving rivers. leaves may be buoyed up almost indefinitely by surface tension (Spicer, 1981 ), whereas whole rafts of plant debris can be carried along, the woodier elements supporting the more fragile and more easily saturated components, even under flood conditions (Berry. 1906). I t is reasonable to assume, therefore, that channel deposits will contain a mixture of plant detritus derived from varying distances upstream. At any given site, however, unless there is evidence for the stranding of a “raft” of vegetation, allochthonous elements will be greatly diluted by material derived from locally growing sources. Levee deposits form naturally when floodwaters. carrying sediment, overtop the rivcr banks and spill out across the floodplain. Release from the confines o f the channel immediately reduces the flow rate, and sediment is depasited lateral to the channel. Successive floods build up a levee that is highcst near thc channel and thins towards the floodplain. This is because the coarsest. bulkiest sediment falls out of suspension first, followed by successively tiner materials as the water flows away from the channel. Levees are composed of laminated sands and silts marked with ripples, climbing ripples and small scours. In vertical section perpendicular to the channel axis they are characteristically wedge-shaped. Because levees are mostly subaerially exposed and relatively well drained between floods, they support different plant communities than the surrounding alluvial swamps (Gastaldo, 1985a,b,c). Oxidation and root penetration tend to destroy most deposited debris, and. in general. levees are poor sites of preservation except, perhaps. for large logs (Gastaldo. 1989; Gastaldo o t LII.1989). In her comprehensive and significant study of fluvial margin litter in paratropical forest environments of southern Mexico, Burnham ( 1 989) reported that low lying areas close to channel margins, the point-bar and levee forebanks. exhibit low species richness and tend to be homogenous. This homogeneity throughout Burnham’s study area must in part be due to fluvial transport mixing of community diversity along the river course. Litter samples reflected well the immediate vegetation in all the subenvironments studied (channel, forebank. levee, back levee), but only slightly less well represented was the local vegetation. As might be expected, the regional flora was the least well represented in all sites because of local dilution effccts. Levee samples represented strongly their own immediate and local f o r a s and back levee sites were more similar to other back levee sites than to other subenvironments. Among Hurnham’s conclusions she pointed out that although within-subenvironment collections were biased, overall and taken together the subenvironments studied yielded a physiognomic signal that reflected well the climate under which the vegetation was growing. Provided that litter collections become incorporated into the fossil record with minimal species (and

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organ) dependent losses, and assemblages from a range of subenvironments are studied, the fossil record is capable of yielding reliable palaeoclimatic signals. This conclusion supports the approach adopted by Spicer and Parrish (1986) and Parrish and Spicer (1988) of multiple facies sampling so as to minimize errors in palaeoclimate reconstruction when strong facies/assemblage association occurs. Crevasse splay deposits are formed when the natural levees are breached in time of flood. The lateral channel that results transports sediment through the gap in the levee and out onto the floodplain. Viewed from above, crevasse splay deposits are commonly fan-shaped with the narrowest portion at the levee breach. The sediments themselves are usually muds, silts and fine sands-the finer fraction of suspended load highest in the river water column. The sediments also tend to become finer away from the point of levee breach. Typically, standing vegetation of the back levee, lateral swamps and floodplain is inundated by the splay deposits. Tree bases may be preserved in situ (Allen, 1970; Gestaldo, 1986a, 1987a), and forest litter may be buried or incorporated into the sediments (leaves are often “rolled” within the sediment matrix), and mixed with river-transported riparian debris and detritus from the levee community. At the sediment-water interface of a crevasse splay in the modern Mobile Delta, Gastaldo et al. (1985) observed that of the 37 taxa identified to species, 34 were not community members of the local vegetation. Rather they were members of either the levee-alluvial swamp or “Pine savanna-bay forest-upland” communities. Only 16% of the recovered macroflora represented local vegetation (Gastaldo, 1985). The speed of burial, the relative fineness of the sediments, and the potential mixture of communities represented, make crevasse splay deposits extremely valuable for obtaining an overall picture of regional floodplain vegetation. This “bulk sample” is particularly useful for palaeoclimatic interpretations, provided the various source communities represented can be resolved by comparison with other more specific, but more local, community samples in other sedimentary facies. The complexity of crevasse splay assemblages is, as yet, poorly understood and more work is likely to yield significant benefits. Floodplain deposits are formed by several processes depending on the nature of the fluvial regime. Low on the floodplain, frequent “levee topping” spills out fine-grained sediments, typically clays and silts, in wide sheets. Here levee, crevasse splay and floodplain deposits may be difficult to differentiate because they are all aspects of the same depositional process. Plant assemblages are similarly complex, but, in general, samples of the interfluve predominate over large areas. Unfortunately such deposits tend to be thin, and subsequent rooting activity and oxidation often destroy any potential plant fossils. Occasionally though, highly siliceous or calcareous seeds may survive (Wing, 1984). However, in floodplains that are waterlogged for most of the time, organic shales or muds typical of marsh environments develop, and delicate, mostly autochthonous, plant parts may be preserved (Wing, 1984).

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ROBERT A. SPICER

Channel migration and relocation (avulsion) over time rework most of the floodplain sediments. This tends to limit the preservation potential of floodplain and interfluve vegetation, and often the only insight into the nature of regional, non-riparian, vegetation may be gained by looking for ubiquitous elements in all the preserved facies. Abandoned channels are a common feature of many fluvial systems. Channel abandonment may occur by meander neck cut-off (so forming “OXbow” type lakes), and by avulsion. Ox-bows can be recognized by their arcuate or crescent shapes, whereas avulsion and chute cut-off produces less curved, more linear deposits. The base of a channel cut-off deposit is usually erosional into the underlying sediments and may contain remnant channel bedload material (Fig. 14). This is often overlain by finer sediment representing the waning flow associated with abandonment. Single-event abandonment is unusual and there may be several periods of reactivation before the channel becomes effectively isolated from the main river. Flood events introduce silts and sands from time to time, and quiet phases between flooding are characterized by fine-grained, laminated sediments typical of lakes. These lacustrine-type sediments may internally fine upwards, but, in general, upward fining is a characteristic of the sedimentary package as a whole. Plant material can be introduced into a channel cut-off, setting throughout the period of infilling. In the basal sediments, riparian debris typical of lag .deposits may be found, passing up into isolated remains of less robust material that was in suspension in the channel at the time of cut-off, or introduced phases of reactivation (Fig. 14). Laminated sediments of quieter periods are likely to contain detritus from communities immediately marginal to the cut-off. In general, low relief and restricted catchment area mean that permanent streams draining into cut-offs are rare, and therefore so too are fluvio-lacustrine deltas. As infilling of the abandoned channel proceeds, water depth diminishes and aquatic communities develop, contributing their own detritus to the potential fossil record. The final phases of infilling are often marked by the development of marsh/swamp communities, and the channel cut-off deposits may be capped with autochthonous organic shales or even coals. Abandoned channel fills including ox-bow lakes, provide a rich source of often exquisitely preserved plant material (Potter, 1976; Crepet and Daghlian, 1981). However, the complexity of the infilling processes demands that detailed sedimentological analysis is required in order to differentiate the contributing communities.

VII.

LACUSTRINE ENVIRONMENTS

Lake basins form in a variety of ways, and the nature of the basin and surrounding topography profoundly affect the nature of the potential fossil

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record they contain. Lakes are so variable that no single suite of sedimentological characteristics is diagnostic of lake deposition. However, several features are more likely to form in lakes than in other environments. Compared to fluvial deposits, lake sediments are laterally more continuous and uniform in thickness. In general they contain fine-grained sediments (though there are many exceptions). They also exhibit extensive areas of fine lamination, and any cross-stratification that exists is of a smaller scale than in fluvial units (Picard and High, 1972; Wing, 1987). However, rapid infilling, particularly of shallow lakes, can produce indistinctly bedded units of relatively coarse sediments that are difficult to identify as lacustrine (Yuretich et al., 1984). The extent to which lake margin (and aquatic) communities are accurately represented in lake deposits depends on basin size and shape, height above the lake surface of the various components of the source community, water chemistry, the amount and distribution of aquatic vegetation, and the characteristics of inflowing streams (if any). If the surface area of a lake is small in relation to the length of its shoreline (e.g. drowned valleys, abandoned channels), the amount of plant debris entering the lake per unit area of lake surface is large, because all parts of the lake are only a short distance from the source vegetation. Furthermore, because the rate of diffusion of oxygen across the air-water interface is a function of the area of the interface (Hutchinson, 1957), the lake tends to become anaerobic with such high organic input per unit surface area, and the preservation potential of the deposited material increases. Source height above the lake surface and distance from the shoreline are critical factors in determining whether or not particular plant parts and taxa are likely to be transported by wind to the lake surface (see Section 1II.B). Spicer (1975, 1981) and Roth and Dilcher (1978) observed selective wind transport to lakes of canopy leaves favouring small, dense “sun” leaves. These leaves are produced at the top of the crown, are exposed to higher wind energies, and are therefore blown further, than “shade” leaves which are produced in the canopy and trunk space. This effect is likely to be most marked where lake width is great in relation to crown height. In such a lake the sediments distal to the shoreline are enriched by sun leaves from canopyforming taxa, and provide a most unreliable sample for community reconstruction and palaeoclimatic interpretations (Spicer, 1981). In such open lake-bottom environments selective biotic degradation of the less robust elements (e.g. shade leaves) is likely to further enhance the bias in favour of “sun” leaves (cf. Heath and Arnold, 1966). Montane lake basins can form as the result of tectonic activity, erosional processes (such as the movement of ice), o r the damning of valleys by slope failure or volcanic activity. The preservation potential of glacial lakes is low because they are generally in an erosional regime, but they frequently survive long enough to be useful for Quarternary studies. The greatest preservation

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potential is found in those lakes resulting from volcanic activity, because the processes that initially dammed the valley can also cap and seal the deposit against subsequent erosion (e.g. Clarkia and Florissant (Smiley and Rember, 1985; MacGinitie, 1953)). Because these lake deposits provide critical insights into not only ancient plant community structure but also vegetation dynamics, they will be treated separately. Isolated lakes ( i t . those with no inflowing or outflowing streams) accumulate plant debris from only two sources: the aquatic vegetation in the lake itself and those communities growing immediately around the lake margins. Low inorganic sedimentation rates are a feature of isolated lakes in that supply is limited to slope wash and surface run-off, aeolian transport. volcanic ash falls, or biogenic sources such as diatom frustules. Although the sediment is usually fine-grained, and therefore ideal for preserving morphological detail, slow influx of sediment inevitably exposes organic material to degradation. Organic deposition accounts for a significant proportion of sediments in isolated lake basins. As infilling proceeds, the ratio of lake perimeter to surface area increases, thus raising the preservation potential of the organics as the system becomes more anaerobic. The eventual fate of any lake is the formation of a swamp, and finally, as more organics accumulate, a forest may develop which is indistinguishable from that which is regionally dominant. Preservation of the debris representing vegetation growing during the final phases of lake infilling is usually poor because of root penetration from subsequent plant communities and oxidation. Aquatic vegetation, although being specialized and of limited palaeoclimatic value, tends to oxygenate the lake water and thereby contribute to the destruction of potential plant fossils. It also traps inwashed (by surface run-off) or inblown plant parts from the lakeside vegetation and prevents forest debris from entering the deeper, and often more anaerobic, parts of the lake. Aquatic macrophytes also increase the abundance and diversity of benthic fauna in the lakes by providing food and shelter (Rau, 1976). The extent of aquatic communities is therefore of particular interest to the taphonomist. Rooted aquatic vegetation tends to flourish (assuming a suitable water chemistry) where water depth is shallow (less than a few metres), water flow is moderate to non-existent, and sedimentation rates are low. Evidence for abundant aquatic vegetation in lacustrine assemblages must imply some considerable bias in the preserved fossil suite because of selective pre-burial degradation, unless other sedimentological evidence indicates that preservation of the assemblage was due to event deposition such as flood or volcanic ash fall. In his review of plant taphonomy in lacustrine sediments Rich ( 1 989) concludes that pollen and spores alone may not give an adequate indication of ancient vegetation and should be supplemented by megafossil data. He also underscores the need to relate sediment type to assemblage composition.

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Ib) m i m g

BOTTOMSET

Fig. 15. Water flow fields over a fluvio-lacustrine delta. See text for details. (Modified from Jopling, 1965a).

Ox-bow lakes have received comparatively little taphonomic attention, but Gastaldo et al. (1989) provide a detailed insight into plant deposition within a Holocene ox-bow lake of the Alabama River. In a transect from backswamp to levee it was clear that the lake sediments themselves preserve leaves as impressions together with organic remains of wood bark, and fructifications. In a separate paper Gastaldo (1989) suggests that in subtropical/ temperate environments such as the Mobile Delta, Alabama, the depositional environment most likely to yield bedded assemblages is in the abandoned channels. A. FLUVIO-LACUSTRINE DELTAS

Perhaps the most valuable lake deposits for the plant palaeoecologist are deltas formed at the mouths of inflowing streams. Not only is the preservation potential of the organic material high because of high sedimentation rates, but also the processes that form fluvio-lacustrine deltas produce plant assemblage patterns that can be used to interpret spatial and temporal aspects of the source vegetation (Spicer, 1981; Spicer and Wolfe, 1987). Upon encountering the relatively static lake waters, the energy of the flowing stream water is dissipated in turbulent flow, the capacity of the stream to transport sediment falls, and deltaic deposits accumulate. Provided that there are no substantial changes in lake level, and the densities of the stream and lake waters are similar, a classic Gilbert-type delta (Gilbert, 1885, 1891) results in which the lake sediments are overlain sequentially by distal deltaic deposits known as bottomsets, followed by toesets, foresets (representing the main part of the delta slope) and finally topsets, which are in effect streambottom sediments. In general the sequence fines upwards and the delta profile is marked in vertical section parallel to the direction of delta advance (progradation) by cross-bed laminations making up the foresets, toesets and bottomsets (Figs 15, 16a). A general model for the formation of this type of delta was proposed by

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Fig. 16. (a) Modern fluvio-lacustrine delta deposits at Trinity Lake, northern California. showing hottomsets. toesets. foresets, and topsets; (h) foreset deposits formed in a lateral lake bordering the Rio Magdelena. Chiapds. Mexic-vertical height of the deposit approximately 3 m.

Jopling (1963, 1965a,b) based on laboratory flume experiments using sand. Jopling envisaged delta deposition by describing the trajectories of individual sedimentary particles as they traversed changing flow velocity fields (Fig. 15). The first field, the “zone of no diffusion”, can be thought of as residual stream flow; following this, particles enter a “zone of mixing” where large scale eddies diffuse the stream energy; and lastly, they enter a zone of reverse circulation where particles are swept back towards the base of the delta slope. A line of zero velocity separates the second and third zones. The point of

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deposition of any given particle (and hence eventually the vertical delta profile) will depend on ( I ) stream depth in relation to lake depth, (2) the settling velocity of the particle, and (3) the velocity of the stream. In particular, the position of the particle in the stream water column as the particle passes over the top of the forest slope and the residence time in the different flow fields are critical factors that determine patterns of deposition.

I . Lowenergy Systems Although originally devised for inorganic particles, Jopling’s model can be used to explain sorting of plant debris in fluvio-lacustrine deltas (Spicer, 1980; Spicer and Wolfe, 1987). Spicer (1981) investigated the accumulation of plant debris in a small, low-energy environment at Silwood Lake, Berkshire, England, and found two distinct leaf beds: one below the delta deposits, representing predominantly lacustrine margin plants, and one at the top of the foresets and in the topsets, representing stream-transported material (Fig. 17). In this system the inorganic sediment fraction was mostly composed of flocculent ferric hydroxide/oxide that had a settling velocity much less than that of the saturated organics. Low stream velocities ( < 1 .O m s - I ) meant that whereas the flocculent inorganics were transported in suspension and as bedload, most of the plant material was moved as bedload only. Consequently the point of greatest organic sedimentation rate was at the top of the foresets, so forming the upper plant bed. The flocs were carried further into the lake basin to build up the delta profile. Progradation of the delta front buried lake-bottom plant accumulations derived primarily from lake-margin communities but also from riparian vegetation upstream, some elements of which were only partly saturated (therefore floating or with a low settling velocity) as they passed over the top of the delta slope. Rapid deposition associated with deltaic sedimentation will bury lakebottom organics and protect some components from the destruction they would otherwise suffer. A similar effect can also be seen in lake sediments normally beyond deltaic influence. In Spicer’s (1981) study, cores revealed that a stream flood event had injected coarse sediment into the lake and produced an upward fining sand-silt-clay horizon that had preferentially preserved taxa normally prone to degradation. Not only did the sand horizon cap lake-bottom accumulations in which partial degradation had already occurred, but also relatively fresh leaves that washed in with the flood sediments became saturated and sank during the time the finer fractions were settling out. These leaves were then buried by the fines before substantial decay could take place (Fig. 18). This example underscores the importance of detailed, high-resolution stratigraphy when interpreting plant assemblages. Plant parts incorporated in an upward-fining cycle that is the result of a single short-term event are likely to be minimally biased by biotic degradation processes. Within the upper plant assemblage, Spicer (1981) was able to map the

136

ROBERT A. SPICER R a n 01 I k a l l y derived leaves

\1

\1

C

- -

*--..---

Vector represenling !he rate 01 sediment depOsilion

Vector representing the late 01 leal deposiliun

Fig. 17. Vector model showing deposition of binary leaf beds in a low-energy Ruvio-lacustrine environment. The lower leaf bed is predominantly derived from sources local to the lake while the upper bed is enriched with stream-transported elements.

lateral distributions of both whole and fragmented leaf taxa, and by using multivariate statistical techniques was able to resolve populations of leaves derived from upstream sources as distinct from more local lake-margin communities. This pattern was most strongly demonstrated in fragmented material (because mechanical fragmentation primarily occurs during stream transport) and led Spicer to propose that analysis of fragmented fossil material was as important in palaeoecological studies as the study of more complete “museum specimens”. So strong was the pattern within the upper leaf bed that in certain instances the position of individual trees relative to the depositional site could be predicted accurately. The two plant beds clearly reflect their separate origins. Plants within the communities local to the lake are represented most strongly in the lower bed, whereas plants in communities at more distant locations are represented in the upper bed. Not only does the species composition differ, but so also does the type and extent of degradation. Leaves in the lower bed will have been primarily transported by wind and subjected to minimal water flow stresses. Consequently the leaves of the lower bed will mostly suffer skeletonization and massive tissue loss produced by biotic degradation. Leaf material in the upper bed, however, will be prodominantly characterized by the angular tears and breaks typical of mechanical degradation. The disparity in species composition between the two beds is not constant. As the delta progrades, its surface will become progressively colonized by various plants as a hydrosere develops. When mature, the delta-top community may well have a composition similar to that surrounding the lake margins (for example, in modern temperate situations Typha, Salix and Alnus are common elements in both environments). Delta vegetation filters

FORMATION A N D INTERPRETATION OF PLANT FOSSIL ASSEMBLAGES DEPTH, IN ORGANIC R E M A I N S METRES

0.0 Leaf B e d 1

0.2

Few leaves dispersed through sediment

0.4

Leaf Bed 2

Well-preserved leaves

INORGANIC SEDIMENT T o p 1.0c m Fe-+hydroxide/ oxide flocs plus some coarse s i l t sized quartz grains Fe++iron-rich sediment as a black semiliquid mud. Clay minerals more o r less absent throughout t h e core

0.6

0.8

Roots in growth posit ion

137

Angular pellets 0.5 c m diameter composed o f same sediments as m u d

1.o

1.2

Black m o r e or less gelatinous m u d Sand layer o f reworked Bagshot sands

Poorly preserved leaves

1.4

Occasional leaf layers

1.6

Fibrous layer remains of aquatic plants

1.8

Roots in g r o w t h posit ion

2.0

Black gelatinous, ironrich m u d

More o r less undisturbed Bagshot sands

Fig. 18. Typical core through the low-energy Huvio-lacustrine delta at Silwood Park, Berkshirc. England. showing the positions of thc lower ( I ) and upper (2) leaf beds in relation t o sediment types. and the position of lcaf horizons associatcd with a high energy influx of sand bctween 1.2and 1.4mdepth.(FromSpicer. 1981).

out detritus from upstream communities (McQueen, 1969) and contributes its own litter to the stream so that in time the composition of the upper plant bed will become similar to that of the lower bed. Progradation of the delta also increases the ratio of the lake perimeter to its surface area. The preservation of organic material increases, and the plant beds may well thicken (Fig. 19). This pattern of assemblage formation and basin infilling has important im-

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ROBERT A. SPICER

Fig. 19. Block diagram showing the development of a binary leaf bed in a lateral lake system. (Modified from Spicer and Grrer. 1986).

plications for the understanding and reconstruction of ancient communities. Vertical sections through the infilled lake parallel to the direction of infilling will reveal two distinct beds (Fig. 20), differing in species content, which reflect the composition of spatially separated source communities and the successional development of hydrosere vegetation. In this case vertical changes in species composition between assemblages does not reflect changes in vegetation with time (the usual interpretation) but contemporaneous spatial distributions. Temporal developments are reflected in lateral changes in species composition within single beds. 2. High-energy Systems The formation of plant megafossil assemblages in fluvio-lacustrine deltas fed by high-energy streams was investigated by Spicer and Wolfe (1987). Here quite a different pattern of plant deposition was seen, but one equally compatible with the Jopling model as that noted in the Silwood study. Six deltas were studied, each at the mouth of separate drainages surrounding Trinity Lake, northern California. The bulk of the deltaic sediments was deposited during floods in 1964 and 1973 and consisted of gravels, sands and silts. Typically, plant material was deposited throughout the deltaic sediments, but was often concentrated in the toesets and foresets. Hydraulic sorting was in evidence, and material with the highest setting velocities (seeds and fruits) was well represented in the foresets, whereas plant parts with low settling velocities (e.g. moss fragments) were found in bottomsets. Toeset deposition was also enhanced by collapse of foreset slopes. In this situation the inorganic sediment had much higher settling velocities than that of the plant debris, and the flow velocities that transported the sands and gravels to the lake also maintained most of the plant material in suspension until it had passed over the top of the delta slope and had fallen into the zones of mixing and backflow (Fig. 21). Although the binary plant bed pattern seen in the Silwood study was not formed, and consequently in-

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a Direction of infilling P

N,>>NL

Upper leaf bed

N,>>

ND

Lower leaf bed

b

Lower leaf bed

Fig. 20. (a) Diagrammatic representation of variations in species composition between upper and lower leaf beds during lake infilling-N,, is the number of leaves derived from distant sources and N, is the number of leaves derived from local sources; (b) as infilling progresses the difference in species composition, represented as a distance measure D, decreases as the litter from distant sources is filtered and diluted out by the developing delta community. (From Spicer, 198 I ).

formation on the spatial distribution of taxa in the source vegetation was not preserved, the overall composition of the plant debris accurately reflected the overall aspect of vegetation within the drainage area. Although hydraulic sorting concentrated certain elements in different parts of the vertical delta profile, sampling of all parts of the delta complex yielded examples of all types of plant organs, including woody roots of the stream side and possibly forest taxa. During the violent weather that often accompanies flood events, fresh materials may be stripped from plants and incorporated into the floodwaters. At the same time, stream-bank erosion introduces large quantities of forest-floor litter and undercuts whole trees which eventually can also contribute to the potential fossil assemblage (Spicer, 1980). The flood transport of fresh material, forest-floor litter and plant debris already in the river system means that when the plant debris arrives at the delta (or other depositional site) it will be in a variety of states of saturation and will exhibit a larger than usual range of settling velocities. This precludes any particle-by-particle predictions of assemblage build-up, but useful generalizations can be made on a statistical population basis, as witnessed by the observed hydraulic sorting of moss fragments and seeds. The six drainages studied a t Trinity Lake (Spicer and Wolfe, 1987) supported a variety of vegetational communities. Three drainages (Mule, Strope,

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ROBERT A. SPICER

Lake

c

- -

VPl I,,!

11.,,11~,,.,111111)

It,<.

,,It,.

,/I

\1.<11111*.11,

,IC,,L,\

,,I,,

n

- ....- ~,.,,r,.w,,,,,,q $11,. In,,. ,It 1vnt Fig. 21. Vector diagram showing leaf deposition in a high energy environment. (From Spicer and Wolfe, 1987). vr,1111

11~.111>\1!11111

and the East Fork of Stuarts Fork) originated at high altitude (approximately 2500 m above sea level and 1750 m above the lake level) and the vegetation reflected the altitudinal range: two drainages (Feeny and Bragdon) drained in an easterly direction from intermediate altitude, and one (Buckeye) represented relatively low altitude vegetation that had been selectively logged and was therefore species-poor. The two east-west trending drainages supported markedly different vegetation on the north-facing and southfacing slopes, the south-facing slope being more xeric. Of the 1,043,000 identifiable plant fragments that were studied from the six drainages, only one, an abraded female cone scale of Pinus halfouriana. could be unequivocally related to the high-altitude communities. Nevertheless, correspondence analysis of the data showed clearly that the deposited debris in all cases distinguished the drainages from each other and therefore reflected to a large extent the source vegetation within each catchment area.

VIII. FLUVIO-MARINE DELTAS A N D ESTUARIES A large fluvio-marine delta provides a mosaic of individually recognizable depositional environments (Fig. 22) in which plant material can accumulate and have a high preservation potential. Although in crude terms fluviomarine deltas are similar to those in fluvio-lacustrine settings in that they have bottomset, foreset and topset units, fluvio-marine deltas tend to be considerably larger and have a geometry and internal structure controlled by sediment supply, density differences between the river and marine waters,

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Fig. 22. Diagram showing the relative positions of fluvio-marine deltaic sub-environments.

tides, currents, winds, and changes in relative sea level brought about by compaction of the delta sediments, tectonic activity or climatic changes. Where sediment supply is low, and/or sediment removal from the river mouth by marine currents outstrips supply, deltas fail to develop and estuaries occur. It is abundantly clear from our experience of the modern world that climate plays an important role in determining the type of vegetation that develops in and around any given depositional setting, and deltas are no exception. What is exceptional about deltas is the control that vegetation has on the development of the delta geometry (and therefore the mosaic of subenvironments that is formed) by binding and trapping sediment. Because of the complexity of fluvio-marine deposits it is meaningless to consider them as single depositional systems. Instead it is more useful to consider the subenvironments from the point of view of the assemblages they are likely to contain. Each subenvironment yields assemblages reflecting a range of selection biases and therefore any analysis of regional vegetation and climate must be based on samples from as many subenvironments as possible, preferably coupled with a knowledge of what those biases are likely to be. A. PRO-DELTA SLOPE

This is made up of the very fine sediment (clay or silt) that is carried the fur-

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thest out to sea and is therefore subject to the effect of marine currents. The sediments may show evidence of low-energy current flow in the form of ripple cross-laminations, but bedding may be destroyed altogether by burrowing organisms. The extent of biodegradation depends on the amount of dissolved oxygen in the water and the rate of sedimentation (Gould, 1970; Morgan, 1970). In general only very finely comminuted plant debris, pollen/ spores or microscopic cuticle fragments are found (if anything at all is found) in these sediments. Any pollen assemblages that are recovered are likely to contain a very strong reworking and/or taphonomic bias introduced by differential long-distance transport and reworking of near-contemporaneous sediments within the delta complex. The exception to this is when gravity slumping of the delta slope occurs and plant debris is transported from near-shore environments in a turbidity flow. Significant amounts of delicate terrestrial material can be transported and buried rapidly in this way (Spicer and Thomas, 1987). As in fluvial systems, fresh material is remarkably robust and can easily survive such treatment, but a feature of a turbidity flow is that entrained particles are carried along as if on a fluidized bed and suffer comparatively little abrasion. Recently I examined a pinnule of the fern Weichselia, charcoalified in a Cretaceous fire, and transported to the sea and then down the continental shelf in a turbidity flow off Spain before being recovered from an ODP core (Leg 103, site 641, hole C). Similar low-abrasion phenomena have been observed in animals (Allison, 1986). Delta front or foreset deposits characteristically dip seawards and consist of mixtures of fine sand, silt and clay. Bedding usually consists of parallel flat laminations, and because of high sediment influx, bioturbation is rare (Allen, 1970; Kames, 1970). As with the pro-delta environment, plant debris is usually finely comminuted (with the exception of larger, woodier material).

B. DISTRIBUTARY MOUTH BARS

These typically sandy upward-coarsening deposits form at the mouths of distributaries (Morgan, 1970; Allen, 1970). Although arcuate convex to the ocean, as the delta progrades, the sedimentary body that results may be elongate. In marine settings plant debris is usually highly fragmented (but in some cases identifiable) and most likely to be preserved in the basal finer sediments. Bioturbation and chemical and microbiological decay agents reduce much of the potential megafossil plant matter to “unidentifiable” hash, but horizons of more or less whole plant parts (including leaves) can occur as the result of event deposition (Gastaldo et al., 1987). These assemblages are a mixture of autochthonous remains and debris transported from nearby and distant (0.5-1 .O km) sources.

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Fig. 23. Mangrove community on the Yucatan Peninsula, Mexico, with minimal litter.

C. TIDAL FLATS

The extent of tidal flat development depends on the tidal range, adequate sediment supply (usually silts and clays) and degree of shelter from current and wave action. In modern cool and temperate climates, tidal flats tend to support only open herbaceous vegetation (Holyoak, 1984; Styan and Bustin, 1983), but in tropical regimes, extensive colonization by mangroves occurs, and this affects sediment accretion (Bird, 1986). Bioturbation is extensive in tidal flat environments and faunal activity may remove all traces of litter under mangroves (Fig. 23), and although in the subsurface the sediments may be highly reducing and organic-rich (Raymond, 1986), they often produce clay rather than peat horizons (Coleman et d.,1970). Covington and Raymond (1 989) discuss the possibility that mangrove peats, where they occur, might have a higher proportion of root debris preserved than shoot remains because initially a higher proportion of the plant is in the form of root biomass. Furthermore the root mats themselves exclude aerial debris from entering the sediments long enough for such debris to be removed by scavenging and decay. Tidal channels exhibit point-bar-type sedimentation with upward fining sequences and ripple laminations (Allen, 1970). Flaser bedding, where silts and clays alternate in fine laminations produced by tidal ebb and flow (and mud drapes similarly produced), may also occur (Allen, 1970), but the channels are generally marked by slightly coarser sediment than the surrounding flats. Scheihing and Pfefferkorn (1984) found, by means of experiments with colour-coded palm seeds and winged seeds, that in the Orinoco Delta, tidal

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cycles were extremely important in winnowing and sorting plant debris. The action of successive tidal cycles tended to concentrate the more robust diaspores and were probably as important as flooding in producing plant assemblages. D. INTERDISTRIBUTARY EMBAYMENTS

These are relatively sheltered environments between actively developing delta lobes. They are best developed in rivers with high sediment load that empty into a water body with little current or wave action. Sediment input into the bay is relatively low except when it is inundated by crevasse splays. The plant material that tends to accumulate is highly comminuted by mechanical degradation as it is transported downriver and around from the distributary mouths. Much of the material that is deposited is destroyed by biological activity, but any that does survive into the fossil record is likely to represent both local and upriver communities (Gastaldo, 1985). Gastaldo et al. (1987) have investigated the plant debris in a crevasse splay system in the Chacaloochee (interdistributary) Bay of the Mobile Delta. Although this detailed and highly significant study documents a single event in a single delta, the main conclusions are likely be be applicable widely. Differential taxon- and organ-dependent degradation, and differential sorting based on size and density, mirrors that noted in lacustrine systems (e.g. Spicer, I98 I; Ferguson, 1985), but assemblage composition reflects geographically more widespread source areas. Potential megafossil plant horizons occur in distributary mouth bars, as peat shoals, and in channel bottoms associated with crevasse splay systems. Crevasse splay accumulations in general consist of autochthonous rooted sediments and/or poorly developed soils admixed with under-represented debris from locally growing lower delta plain plants, and over-represented material derived from distant upper delta plain communities, and even debris from outside the delta itself. Gastaldo et al. (1987) suggest that most litter beds represent channel-bottom accumulations buried during the initial phases of flooding. Fluvial, tidal and windgenerated currents mechanically degrade much of the organic material that accumulates in shallow areas with low clastic input. The detrital peats that form in these areas are rich, therefore, in the more robust elements such as wood and periderm detritus. Identifiable material does occur and has a composition similar to that seen in the distributary mouth bars and reflects a similar range of sources. E. BEACHES

Considerable amounts of organic material may accumulate on beaches, some (logs and large diaspores such as coconuts) perhaps having undergone trans-

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port of several thousand kilometres by ocean currents. In most instances very little of this material ever survives into the fossil record because of degradation by wave action, biodegradation and high oxygen levels in the generally well-sorted coarse sediments that result from tide current and wave winnowing. In sand or silt beaches bedding is often laminated and dips seawards at a low angle, and finely comminuted plant hash may be distributed over the bedding surfaces. In deltaic environments beach ridges can accumulate large quantities of finely comminuted allochthonous woody detritus. Allen et al. (1979) observed extensive deposits of such material over 2-m thick in the modern Mahakam Delta, but although a high-ash coal may result from such accumulations, very few of the larger fragments would be identifiable and any palaeocommunity signal would be difficult to interpret. However, this terrestrially-derived organic material has been proposed as the source of hydrocarbons for oil and gas genesis (Risk and Rhodes, 1985; Durand er al. 1986). F. LOWER DELTA PLAIN MARSHES

In modern cool and temperate regimes the first plants to colonize subaerially exposed deltaic sediments tend to be herbaceous, and any potential megafossils, because of their non-woody nature, are rapidly degraded. Nevertheless, even distally a discontinuous patchwork of thin peats may be formed (Styan and Bustin, 1983). These peats are often rich in sulphur derived from marine influences. As the sediment thickness increases, fresh-water flushing and the establishment of non-saline groundwater lenses above more saline porewater give rise to fresh-water swamps, which again, in temperate regimes, are mostly herbaceous. Apart from the most distal portions, the lower delta plain marshes are subject to frequent crevassing and flooding of the river system. As a consequence marsh deposits of thin herbaceous (sedge/grass to Sphagnum) peats are intercalated with fluvial deposits that may exhibit a range of grain sizes (Styan and Bustin, 1983). However, the overall sediment aspect will be finegrained. In ‘the past the role of herbaceous plants in colonizing such environments may not have been strictly analogous to that of the present day, and marsh development, and the resulting fossil record, may have been correspondingly different. Even in the absence of trees, rooting of the marsh plants tends to destroy both bedding and recognizable plant parts (Gallagher and Plumley, 1979). Any surviving plant debris will be finely disseminated. The intertwining of roots forms a coherent rhizomatous mat (Gastaldo, 1986b) which is resistant to erosion. When erosion does occur, the mat breaks in a characteristic fashion which may be useful in interpreting ancient environments (McManus and Alizai, 1983). These mats may form the foundation for the

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accumulation of true peats or organic-rich muds, depending on the sedimentation regime. If sedimentation rates are high, however, and more or less keep pace with colonization, evidence of even herbaceous elements will be preserved in the form of stacked rooted sediments and organic-rich incipient paleosols. In modern, warm temperate to subtropical lower delta plain marshes, woody vegetation predominantly composed of both conifers and angiosperms gives rise to organic-rich sediments and in situ peats (Gastaldo, 1986~).The preservation of identifiable compression megafossils in such environments is in large part dependent on clastic input. The development of dense herbaceous cover tends to filter out plant debris brought in by floods and crevasse splays (Scheihing and Pfefferkorn, 1984), and therefore, away from the channels, any preserved remains in lower delta plain marsh environments are likely to be of extreme local origin or autochthonous. Within the area affected by crevasse splays, the assemblages are likely to reflect mixed source areas as documented by Gastaldo et al. (1987). G. UPPER DELTA PLAIN MARSHES

The upper delta plain environments of most modern deltas tend to be wooded and floristically more diverse than those of the lower delta plain. In large part this is due to better soil drainage, but even here the water table is close to the surface and extensive organic-rich sediments and peats can develop. In the Frazier River upper delta plain sedge-wood peats develop adjacent to levees (Styan and Bustin, 1983). These peats contain high proportions of material derived from riparian vegetation, including bark and stem fragments admixed with roots and degraded leaf material, while in situ erect tree stumps also occur commonly. Although these peats may be affected by brackish water, marine influences are less than those experienced in the lower delta plain. In the Mobile Delta, Alabama, the upper delta plain is characterized by extensive low-lying alluvial swamps vegetated by Nyssa and Taxodium, bounded by well-developed levees (Gastaldo, 1986c; Gastaldo et al., 1987). Organic-rich sediments are extensive, but true peats are rare. Like levees, the alluvial swamp environment has a low potential for the preservation of identifiable megafloral remains, with the possible exception of prostrate logs (Gastaldo, 1986~).The likelihood of preservation is increased greatly during flood conditions. However, levee crevasse would result not only in high sedimentation but also in a mixed assemblage derived from levee, riparian and swamp communities (Gastaldo, 1986~).Sieving of the alluvial swamp sediments yields a diversity of plant organs, with fragments of angiosperm leaves and branches occurring most commonly. Although Taxodium appears under-represented, entire lateral branches with leaves attached do occur.

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Gastaldo (1986~)notes that this fragmental hypoautochthonous debris could be misinterpreted as a comminuted transported assemblage. However, when in situ tree bases are preserved they are deemed by Gastaldo (1986~)to be a good indicator of clastic swamp conditions. H. DELTAIC LACUSTRINE A N D FLUVIAL ENVIRONMENTS

The patterns and processes of assemblage formation in the other deltaic environments are essentially similar to those previously described for lacustrine and generalized fluvial systems. Differences in assemblage composition reflect the various communities growing on the delta. The significance of deltaic regimes lies in the fact that as the deltaic sediments compact, the delta surface continually subsides, and the addition of further sediment buries and preserves the previously deposited assemblages. Consequently, deltaic deposits account for a large proportion of the plant fossil record and as a result the plant fossil record tends to be skewed in favour of the somewhat specialized communities inhabiting deltaic situations. Clearly an appreciation of the broader setting for individual depositional environments is necessary to differentiate communities on ancient landscapes. I. DETRITAL PEATS

As we gave seen, numerous sites within a large delta complex accumulate allochthonous disseminated plant debris, but deposition appears to be greatest in interdistributary bays, distributary mouth bars and beach ridges. Working in the Mobile Delta, Gastaldo et af. (1985, 1987) assessed the plant detrital organ composition and size fraction within detrital peats. They found that leaf material of both deciduous angiosperms and gymnosperms predominate, whereas bark and wood fragments were subdominant. Local aquatic vegetation contributed only a minor component. Because of the relatively high inorganic component, many of these “peats” would be likely to result in carbonaceous shale rather than coal.

IX. PEAT A N D COAL ASSEMBLAGES All the situations discussed so far have involved an element of plant debris transport and therefore have resulted in allochthonous assemblages. Some coals undoubtedly have an allochthonous origin and examples of allochthonous peats have already been discussed. However, most commercially exploitable coals are autochthonous (Teichmuller and Teichmuller, 1982); the plant remains have become incorporated at the site of growth (roots, plant bases and fallen logs) o r have undergone limited lateral wind transport (leaves,

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reproductive organs, twigs). Potentially a peat deposit can yield a detailed view of the mire community, although the view would be time-averaged because any one sample of peat contains the remains of plants that were growing at slightly different times (e.g. rooting structures penetrate an assemblage of debris derived from plants of different ages). The process of converting peat to coal is one of progressive increase in the relative concentration of carbon as more volatile components are driven off by the combined effects of heat, pressure and time. This coalification process eventually distorts and destroys most identifiable larger plant remains, leaving coal lithotypes and pollen/spore assemblages to characterize the mire communities. Traditionally the components of most bituminous and higher rank coals have been studied either by means of permineralized material occurring in siliceous or carbonate concretions within the coals themselves (coal balls), or compression fossils in clastics associated with the coals. The relevance of clastic-entombed debris to the mire communities has been rightly questioned (Scott, 1977), except where crevasse splays have preserved plants in situ (Gastaldo, 1987a). The environments of coal deposition are many and varied and the relative abundance of certain types of environments have changed with time as a result of fluctuating sea levels and climate. McCabe (1984) gives a useful summary of coal depositional environments and the reader is referred to that work for a more complete treatment than is possible here. However, inasmuch as the depositional environment of the coal affects both the community and the assemblage composition, and is therefore an important component in palaeoecological interpretations, some discussion is relevant here. To a botanist it is probably obvious that coal is a heterogeneous substance because it is derived from vegetation that is also heterogeneous in both space and time, but this simple fact appears to have been traditionally overlooked by sedimentologists and even coal geologists (McCabe, 1984). Because of this attitude, models for coal (peat) formation and coal taphonomy are relatively new. Although climate, in particular an excess of precipitation over evaporation, is important for peat development, the presence of coals does not necessarily imply that the original mires enjoyed warm, wet conditions. The partial decoupling of coals from climate is due to topographic and sedimentary regime effects. The main requirements for peat development are organic productivity that outstrips organic decay, and the exclusion of clastic sediments that would dilute the organics. Decay is limited by anoxia, temperatures in the region of 4°C or below, or low pH. Of these, low temperatures are not usually conducive to coal formation because productivity also is curtailed. However, in extremely seasonal climates, warm summers and cool winters can give rise to exceptionally large coal reserves (e.g. Spicer, 1987). High rates of organic input into standing water give rise to anaerobic and

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Fig. 24. Diagram showing the development of a floating mire at lake margins. (Modified from McCabe, 1984).

acid conditions, and as a consequence the development of specialized mire communities in and around shallow water-filled topographic lows has long been considered to represent sites of potential coal formation. Such lows are found adjacent to rivers on alluvial plains either as linear fluvial margin swamps or as subsidence depressions on delta surfaces. The proximity of these environments to fluvial systems means that the mire communities are subject to frequent flooding, bringing possible disturbance to the community and the introduction of clastics. As a result these topogenous peats are often thin, have a high inorganic content, are laterally restricted, and therefore make poor commercial coals. Flooding and restricted peat depth mean that nutrient status of the community is high (Teichmuller and Teichmuller, 1982), and is not limiting to productivity or diversity, but the quality of the resultant coal is degraded because it has a high ash content. However, clastic input does enhance the preservation potential of recognizable plant megafossils, and the close proximity to levee and riparian communities means that plants preserved in association with the coal are likely to represent several communities. Debris from these communities is likely to be mixed, and the intercalation of sediments demands detailed analysis before any generalizations regarding the coal-forming community can be made. In more open-water lakes such as meander cut-offs, floating swamps o r “quaking bogs” may form (Fig. 24). Floating peats in the Okefenokee Swamp have been described by Spackman et al. (1976) but peats of this kind are widespread and occur in climates ranging from tropical to cool temperate. The peats may progressively develop towards the lake centre from the lake margins, or detached islands of peat may become joined to lake-bottom peats by downward root growth. Eventually the lake surface may be entirely covered and support large trees. Species diversity is often lower in the centre of such peats unless groundwater movement or flooding supply nutrients. The distribution of palynomorphs within such peats, or the coals derived from them, may be complex because of wind-drifted peat rafts, floating and sinking of the peats due to internal gas generation and release, and differential degradation and relocation due to water-flow through the peats. Where precipitation exceeds evaporation/transpiration and no marked dry season occurs, a raised mire or ombrogenous peat may develop. Such peats

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Fig. 25. The development of a lowland raised mire-(a) peat deposition may become initiated in a topographic low and because roots may penetrate to the underlying clastics and/or there is runoff into the depression from the surrounding slopes nutrient status of the mire is high and plant diversity is high; (b) uniformly high precipitation throughout the year sustains peat development above the groundwater table but diversity drops as nutrient status falls due to the meteoric water supply; (c) in a mature raised mire sustained by meteroic water, species diversity and plant stature is low in the centre of the mire but increases towards the mire margins as plant roots penetrate to the clastics and nutrients are supplied to the peat at times of flood-these temporal and spatial changes during mire development are recorded in the peat palynofacies and macerals. Although a lowland setting is illustrated here raised mires can develop in any situation where rainfall is consistently high and temperatures are conducive to plant growth. (Modified from McCabe, 1984).

can occur at any latitude but those most intensively studied from the point of view of the fossil record are in tropical SE Asia. The peat may be initiated in a topographic low, a saline marsh environment or even on elevated slopes on mountains or alluvial fans (Morley, 1981; Hunt and Hobday, 1984), but high rainfall prevents the organic matter drying out even when the peat accumulation exceeds the groundwater level (Figs 25 a,b,c).. As peat continues to accumulate, the vegetation increasingly is supplied only by meteoric water, and nutrient levels decline (Teichmuller and Teichmuller, 1982). Recycling of nutrients within the upper part of the peat occurs and species diversity typically declines both towards the centre of a raised mire and through time as the mire develops (Anderson, 1964a,b, 1983; Coleman et al., 1970; Polack, 1975). These spatial and temporal changes are reflected in changing peat facies (Anderson, 1964a,b; Romanov, 1968; Anderson and Muller, 1975). A mature raised mire is typically domed but may have a flat top and even support lakes (Romanov, 1968). The elevation of the raised mire largely protects it from clastic input except

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at its margins, and as a result raised mire communities may be the source for many of the thicker low-ash coals (McCabe, 1984). Unless permineralization takes place within the peat (see Section XI), the lack of clastics within the coal unit means that very little in the way of plant megafossils will survive in sub-bituminous or higher rank coals. Here the only records of the characteristic source vegetation diversity distributions comprising the coal will be the palynological assemblages, although limited information may be preserved in the distribution of biologically important elements (highest concentrations in the upper part of the seam and to the centre) or the lithotypes. Obviously in order to detect these changes the coal must be investigated on a large scale three-dimensional1y . Peat is very resistant to erosion (McCabe, 1984), and raised mires serve to restrict river courses. As a consequence, rapid lateral changes from fluvial sediments to coal seams may be evident, and if the region is tectonically active, vertical changes may be similarly abrupt. This provides strong juxtaposition of plant assemblages of very different composition, and comparative studies of palynomorphs in coals and clastics could prove extremely valuable, both from the point of view of accurate community differentiation and reconstruction, and biostratigraphically.

X. VULCANISM Vulcanism has played a major role in shaping the plant fossil record. Some of the best preserved “intact” ancient plant communities were entombed as a result of eruptive activity (e.g. the Devonian Rhynie Chert (Kidston and Lang, 1917) and the Yellowstone fossil forests (Fisk, 1976)), as well as a host of allochthonous assemblages (e.g. the Neogene assemblages of the Pacific Northwest of North America (Axelrod, 1964; Graham, 1965; Smiley and Rember, 1985)). Innumerable assemblages are in sediments that contain contemporaneous volcaniclastics (or their diagenetic products) derived from distant volcanic vents. The taphonomic importance of vulcanism to plant palaeoecological studies was recognized long ago (e.g. Hague et al., 1899), and Dorf (1951) published observations on the burial of plant material by Paracutin (Mexico). Little additional work was carried out, however, until very recently when the spectacular and well-documented eruption of Mount Saint Helens (Washington State, USA) stimulated a spate of taphonomic research. The type of plant fossil record preserved in volcanic terrains is related strongly to the type of vulcanism involved. The magma of volcanoes at subducting plate margins tends to be rich in silica, largely because it is derived from melted crustal material, and as a consequence is viscous. This viscosity prevents the easy escape of contained gases and can lead to the build-up of high pressures within the magma pipe. Degassing and eruptions tend, there-

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fore, to be explosive, and the high viscosity of the erupted material results in steep-sided volcanic cones. Such volcanoes are found in the Andes and the Cascade Range of western North America. The violence of the eruptions can lead to massive local vegetational disturbance and the production of large quantities of volcaniclastic sediments which create depositional environments and provide an abundance of sediment for the rapid entombment of potential fossils. The steep slopes also play an important role in sediment shedding from the vent, and the production of mud flows, that can have an important taphonomic role. At the other extreme are the volcanoes found along mid-ocean ridges or over “hot spots” in the oceans. In these cases the oceanic crust is thin compared to crustal thickness at continental margins, and rising magma, mostly derived from subcrustal material and with a low residence time in crustal rocks, is low in silica. This produces low-viscosity magma which typically erupts as rivers of mobile lava that rapidly spread away from the vent and form low domes or shield volcanoes such as those seen in the Hawaiian Islands. These two extremes are bridged by a host of intermediate forms that differ in magma chemistry and morphology as a result of their position relative to continental margins, crustal thickness and chemistry, and relative plate movements. To date most plant taphonomic work has been carried out in terrains related to explosive vulcanism and in particular at Mount Saint Helens (Washington, USA), Nevado del Ruis (Columbia) and El Chichon (Mexico). That other types of vulcanism have been important in contributing to the plant fossil record is obvious, but for the moment interpretation of those deposits depends on extrapolation from the studies of explosive vulcanism, casual observation, and conjecture. A. THE IMPORTANCE OF EXPLOSIVE VULCANISM TO THE PLANT FOSSIL RECORD: CASE STUDIES

I. Mount Saint Helens-The 1980 Eruptions Mount Saint Helens (MSH) is one of a number of volcanoes in the Cascade Range that stretches northwards from northern California to British Columbia. Prior to 18 May 1980 the steep-sided symmetrical cone of MSH rose above the surrounding foothills topography, and the area was drained by the North and South Forks of the Toutle River (Fig. 26a). The flanks and areas surrounding MSH were covered with mature, mixed-conifer forests with angiosperm trees primarily confined to riparian situations or logged areas. In the following account, where I have not referenced published literature, the observations are my own. The mechanics of the eruption have been described in detail elsewhere (Lipman and Mullineaux, 1981) and so only a brief description relevant to taphonomic considerations will be given here.

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Fig. 26. (a) Plinian column eruption of Mount Saint Helens (MSH) on 18 May, 1980 (b) MSH in the middle distance as it was in September 1978, to the east in the distance is another Cascade volcano, Mount Adams; (c) pyroclastic flow down to the northeast flank of MSH.

On 18 May 1980 a magnitude 5 earthquake triggered the failure of the northern flank of the volcano, and as the confining pressure on the magma and cone was released, superheated groundwater within the mountain flashed to steam and the magma explosively degassed. As a result the leading edge of the collapsing flank was propelled northwards initially at more than 200 m s - l (Kieffer, 1981), and within 13 min had fanned out to a distance of 30 km from the vent and destroyed an area of approximately 600 km2 of forest (Fig. 27). Following this lateral blast, and the removal of approximately 2.8 km3 of the mountain, the eruptive column grew vertically to a height of 20 km (Christiansen and Peterson, 198 1) (Fig. 26b,c). The heaviest sand-sized ash particles fell out of the column within a few kilometres of the vent, but the fines settled out over much of the Pacific Northwest to a depth of several centimetres (Carey and Sigurdsson, 1982). In all, the newly erupted material amounted to a volume of approximately 0.2 km3; all in the form of ash, pumice, and more solid blocks of dacitic ejecta.

Blast efects. The dynamics of the blast have been described in detail (Kleiffer, 1981) and from the palaeobotanical point of view several aspects

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Fig. 27. Map of the post 1980 MSH area-the principal lateral lakes are shown in black.

are of interest. Perhaps most important is that comparatively little organic material showed signs of charring. The charring that did occur was mostly confined to the sides of the blast fan and to the lighter fraction (mostly conifer needles), which was carried aloft by convection from the blast cloud. This material was subject to relatively long-distance dispersal, as witnesses reported a rain of blackened needles some 30 km away from the vent. The lack of charring on most tree remains within the blast area is attributable to the fact that blow-down was primarily caused by the impact of relatively cold mountainside. It was only after the initial impact that hot ash and gases swept over the area. At the extremity of the blast area these hot gases melted the epicuticular waxes of standing conifers (Winner and Casadevall, 1981). Proximal to the vent, and on slopes within a radius of approximately 8 km that were directly exposed to the blast, both trees and topsoil were stripped away. On more sheltered slopes, and up to a radius of 12 km on exposed slopes, trees up to a metre or so in diameter (at pre-blast breast height) were snapped a few feet above ground level. In more distal areas, trees were uprooted, blown down with their apices either pointing away from the vent or from topographic features that redirected the blast, and stripped bare of branches (Fig. 28a). Some were buried in valley bottoms by blast material (Fig. 29a). Still further away, trees remained standing but were stripped of branches and bark on the side of the trunk facing the effective blast source (Fig. 28b). At the margins of the blast zone, as the waning energy of the cloud enabled it to rise convectively, conifers were heat-killed and merely stripped of their leaves, which accumulated in abundance in stream point-bar deposits (Fig. 29b). Most of the directionally blown-down trees were on elevated sites and

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Fig. 28. (a) Directional blowdown of trees at MSH showing how at distances of 20 km or so from the vent, the blast trajectory was modified by topography; (b) at the edges of the blast zone, some 30 km from the vent, convective lifting of the blast cloud caused some trees to snap well above the ground while others were blown over but retained lateral branches.

would have little potential for preservation in situ, although the fossil record does yield instances of directional blow-down (Froggatt et al., 1981) that have allowed ancient vent sites to be pinpointed. Some trees proximal to the volcano were baked and fusainized by burial under pyroclastic flows (Fig. 26c), and charcoalification would enhance their preservation potential. However, by far the best record of pre-eruption logs would be in lake and river valley deposits.

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Fig. 29. (a) Riparian vegetation (Salix sp. bushes) and slope trees mixed and buried in valley bottoms by blast cloud sediments approximately 25 km from the vent of MSH; (b) lenses of blast-removedconifer leaves concentrated in small point bar deposits 30 km to the north of MSH in the Green River.

The eruption introduced large numbers of logs into Spirit Lake (8 km north of the crater) directly by blast and indirectly by lake-water surge that scoured the surrounding hillsides above the pre-eruption lake level. Logs with and without attached root systems were represented in the floating log jam that covered approximately two-thirds of the post-eruption lake surface, and which moved around the lake by wind action. Those logs with attached

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Fig. 30. (a) Spirit Lake floating logjam with MSH in the distance as it appeared in 1982; (b) a, North Coldwater Lake; b, South Coldwater valley, as they appeared in August 1982. The MSH debris flow, which dammed both valleys and led to the formation of Coldwater Lake, is shown in the foreground.

roots absorbed water preferentially at the rooted end and many floated and presumably settled on the lake bottom “in life position” (Coffin, 1983; Fritz, 1986). Four years after the eruption many logs were still afloat (Fig. 30a), but their ultimate fate will be burial in lacustrine sediments. Although many large ( > 1.O m diamater) trunks were snapped transversely (Fig. 31a), and showed other signs of traumatic injury (Fig. 31b), buried adjacent to them in the blast deposits were delicate structures such as intact

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Fig. 31. (a) Traumatic blast injury to a mature Pseudorsuga tree approximately 8 km to the north of MSH; (b) volcaniclastics blast-impacted into a tree 8 km from MSH-the scale coin is 24 mm in diameter; (c) female cone of Pseudorsugu, found adjacent to the log in a and lying next to blast-pulverised wood.

female cones of Pseudotsuga menziesii complete with exserted bracts (Fig. 31c). The structure of the blast cloud was complex, and in many respects it acted as a dense fluid. Many of the lighter, more easily transported, plant parts were buoyed up in the cloud and suffered only minor damage. During the post-eruption re-establishment of drainage systems, reworking of this material into sediment traps potentially may provide a moderately complete picture of the pre-eruption vegetation.

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Fig. 32. (a) Vertical aerial photograph of El Chichon taken in 1975 showing the mozaic of natural paratropical rainforest on the summit and slopes, and the cultivated areas in the Rio Magdelena valley (the Rio Magdelena is in the bottom right quadrant of the photograph); (b) lateral lakes, arrowed, along the debris-filled Rio Magdelena as it appeared in March 1984;; (c) El Chichon crater (almost 1 km in diameter), corresponding to the central peak shown in a, and the Rio Magdelena valley, March 1984.

2. El Chichbn The eruptions of El Chichbn, Chiapas, southern Mexico (Fig. 32a), between 28 March and 4 April 1982, produced no lateral blast but provided a suite of depositional environments that in many ways were similar to those seen at MSH.

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The first eruption explosively removed the summit cone that was clothed in paratropical rainforest (sensu Wolfe, 1979). A column of ash and sulphurous aerosol rose to a height of 16.8 km and produced several centimetres of airfall ash over a wide area of southern Mexico. Eventual column collapse produced pryoclastic flows and surges that devastated about 154 km2 of cocoa (Theobrorna cacoa) and coffee (Cogea)plantations, admixed with predominantly second-growth paratropical rainforest immediately around the volcano. Areas of cultivated beans and corn existed near populated areas. Further intermittent activity culminated in two major explosive eruptions on 3 April and 4 April. Detailed descriptions of the eruptive activity are given in Varekamp er al. (1982), SEAN Bulletin (1982), Duffield et al. (1984) and Sigurdsson et al. ( I 985). Apart from the lack of lateral blast, the El Chichon eruptions differ from the 18 May 1980 eruption of MSH in several other respects. Column collapse inundated standing vegetation with hot surge pyroclastics which were mainly channelled along existing drainages radiating from the cone. As a consequence of this, much of the plant material in these drainages was exposed to intense heat ( > 300°C) for periods ranging from days to months while the flows cooled. Entombment within the flows, some of which near the base of the cone were over 20 m thick, prevented air from reaching the organics, and as a result charcoalification occurred either superficially (Fig. 33a) or, in the cases of some large logs, throughout (Fig. 33b), so preserving external morphology and cellular structure in exquisite detail. Although less violent than the lateral blast at MSH, the pyroclastic surges stripped or buried proximal vegetation at El Chichon. At the periphery of surge damage (approximately at a radius of 6 km but dependent on local topography) the surge cloud convectively rose to kill only the canopy trees by heat and mechanical removal of leaves and branches. B. DEBRIS FLOWS

At MSH, blast-ejected material and gravity-slumped mountainside, coupled with groundwater, glacial meltwater and condensed steam, produced a 16-km long debris flow (a lahar) that filled the approximately 1-km wide North Toutle river valley to an average depth of 45 m. The advance of the debris flow scoured topsoil and vegetation from the valley sides and, because the organic material was less dense than the inorganic, it formed an extensive organic “plug” at the leading edge of the flow (Fig. 34a). Over 90% by volume of this wedge was soil and pulverized wood supporting transported whole trees, many of which were upright. Had the US Corps of Engineers not destroyed this deposit in a vain attempt to dam the valley against further mud flows (the dam was overwhelmed), this organic deposit may have been buried by subsequent downstream sediment transport and mud-flows. The

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Fig. 33. (a) Tree base charred by hot pyroclastic flows 6 km from the vent of El Chichon; (b) charcoalified transported log in El Chichon pyroclastic flows. Charcoalification renders plant material inert and thus increases the preservation potential.

advancing debris flow pushed the river waters ahead of it and this water, together with dewatering of the debris flow, produced extensive flooding, sediment transport, and deposition throughout the Toutle drainage (Janda et al., 1981; Pierson, 1985). Downstream of the debris flow, hyperconcentrated stream flow scoured and buried valley-bottom vegetation. Commonly, soil horizons remained intact and flexible saplings remained in situ but with leaves and branches stripped and the trunks abraded to form sharp apical points (“bayonets”)

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Fig. 34. (a) Transported trees at the leading edge of the North Toutle River valley debris flow at MSH-some trees were in life position; (b) blast and/or debris flow-transported block of forest floor containing seeds and rhizomes of pre-eruption vegetation acting as an innoculum for colonization of the debris surface. Photograph taken in August 1982.

pointing downstream. In all there were at least three periods of hyperconcentrated stream flow in the Toutle River drainages (Fritz, 1986) and probably there would have been more had the lakes in the area (see below) not been artificially drained to prevent further flooding. A small eruption in March 1982 melted snow in the crater and resulted in additional hyperconcentrated flow in the North Toutle River valley (Waitt et al., 1983). This prolonged intermittent activity following a violent initial eruption is common in

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Fig. 35. Hypothetical composite section through sediments deposited by successive hyperconcentrated steam flows. a, pre-event soil horizon; b, basal graded gravel; c, horizontally stratified gravels and sands; d, matrix-supported muddy sediments containing pumice blocks and assorted organic debris. In subsequent events the development of a soil horizon will depend on the duration of the time interval separating events, and similarly the concentration and nature of the organics in d will depend on the degree of vegetation recovery. (Based on Fritz, 1986)

explosive vulcanism and potentially provides additional sediments for sealing deposits formed by the initial, and earlier subsequent, events. The lack of a glaciated summit at El Chichon meant that during the eruptions relatively little water was available to form lahars. However, pyroclastic flows dammed the Rio Magdalena for a period of approximately three months until the ponded water, forming a lake over 4 km in length, overtopped the dam. Rapid downcutting by the escaping water eroded the dam in a matter of minutes and a flood of hyperconcentrated stream flow, heated by passage through the still-hot pyroclastics, surged down the river valley. Typical deposits produced by a single hyperconcentrated stream flow event consist of a basal graded, closed-framework gravel overlain by a horizontally stratified gravel and sand (Fig. 35). Capping the unit typically there is a matrix-supported muddy mixture containing large pumice boulders and most of the transported organic debris (Fritz, 1986; Harrison and Fritz, 1982). Not only was this type of deposit seen at MSH, but it was also

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Fig. 36. (a) The fern Pityrogramma calamelanos regenerating from buried and exhumed rhizomes on the slopes of El Chichbn in March 1984; (b) deposits in the Rio Magdelena River valley resulting from the “Agua Caliente” hyperconcentrated stream flow produced by the breakout of the eruption-ponded Magdelena Lake. Cocoa (Theobroma) leaves can be seen protruding from the deposits at the base of the horizontallystratified gravels (cf Fig. 35).

observed at Nevado del Ruiz and occurs in many Tertiary deposits (Fritz, 1986). At El Chichbn a similar type of deposit was formed by failure of the Rio Magdalena pyroclastic dam. In this instance the deposits contained coriaceous cocoa leaves (Fig. 36b). Fritz and Harrison (1985) noted that 5-15% of the transported tree population remained upright during transport, while the remainder were deposited as horizontal logs, often orientated by the flow. The main factor determining upright stability is the trunk length/root diameter ratio. Trees with a ratio of 1 or less are upright stable. Karowe and Jefferson (1987) reported the transport at MSH of a “rafted island” of forested land measuring 10 m by 20 m, and pointed out that unless sufficient exposure is available in fossil situations, such rafts could be confused with in situ forest growth. Differentiating transported from in situ trees is clearly essential for accurate interpretation of ancient communities. Fritz (1986) noted that at MSH even transported trees had small hair roots intact, but larger roots tended to be rigid and were often broken off. In addition the root masses contained boulders and cobbles, so the presence of such features in the fossil record is poor evidence for in-place preservation. While the centre of channels rarely contained anything but transported debris, channel margin and overbank

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deposits yielded mixed transported and in situ trees (but see Karowe and Jefferson (1987)). Growing riparian trees were commonly killed by the heat of the flows (- 70°C) even though they were buried by a metre or less of sediment. Thus their bases and abscissed aerial parts may eventually be preserved. Channel margins therefore provide a mixed assemblage potentially representing several communities and, if local topography is pronounced, several zones of microclimates. Fritz (1986) suggested that if the proportion of upright to prone trees is greater than 15% some, or all, of the assemblage may be in place. However, this must be coupled with a detailed analysis of the position of the deposit with respect to the channel itself, and of associated paleosols (if any). Another factor to be taken into consideration when interpreting fossil tree assemblages is evidence for post-burial continuation of growth, such as the development of abnormal growth bulges and reaction wood (Karowe and Jefferson, 1987). Such features would not be expected to any significant extent in transported trees. Repeated hyperconcentrated stream flow events would rapidly build up substantial thicknesses of superimposed units such as the one described above, each with an upper layer containing organic debris (Fig. 35). The nature of this organic assemblage depends on the amount of material available for burial. Thick units with tree bases and logs are to be expected in deposits produced by the initial eruption, but subsequent deposits may be more sparse, depending on the time intervals between events in relation to the rate of vegetation recovery. Each event may also preserve the vegetation (if any) over which it passed, and comparisons of the buried in situ (as compared to transported) debris may provide data critical to differentiating spatial differences in communities and the dynamics of post-disturbance recovery. Not all debris flows passing through vegetated terrain preserve plant material. The eruption of Nevado del Ruiz in 1985 produced no lateral blast, but collapse of the eruptive column led to pyroclastic flows and melting of glacial ice (Fritz, 1986). The resulting mud and debris flows travelled down drainages for more than 60 km over a vertical distance of 5000 m. The high velocity of these flows apparently pulverized trees that were stripped from valley sides. Deposits some 30 m in thickness could be seen 40 km from the vent, but in the more distal regions the flows spread out as thin (< 1.Om thick) sheets. These distal deposits did contain some transported trees as well as wood splinters, leaf debris and pollen (Fritz, 1986), and smelled of methane and decaying plant matter shortly after deposition. A characteristic of vegetation in volcanic terrains, particularly that in valley bottoms, is that it is prone to repeated disturbance. Even if it were to be demonstrated that superimposed fossil stump fields (e.g. Jefferson, 1982) represented in-place fossil forests, the repeated disturbance is likely to render suspect climatic or ecological inferences based on tree spacing or growth-ring data. Minor influxes of sediment, particularly if hot, are sufficient to elimin-

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ate crops of seedlings and may be difficult to detect after root disruption. Certainly such disturbed “fossil forests” should not be taken as representing more regional “steady-state’’ conditions or as being typical of undisturbed forests (cf. Creber and Chaloner, 1984, 1985; Francis, 1986) without first determining the frequency of disturbance. C. PRESERVATION IN AIR-FALL TEPHRA

Air-fall tephra composed of pumice pieces several centimetres in diameter down to extremely fine ash particles affects a much wider area around a volcano than blast, lahars or pyroclastic flows. The grain size of air-fall tephra generally decreases with increasing distance from the vent and its distribution is dependent on prevailing wind conditions and rainfall. Ash layers are common in many fossil deposits and are used frequently for correlation purposes. However, the extents to which ash fall affects the standing vegetation, and its role in preservation, are discussed only rarely. Studies at MSH showed that several centimetres of air-fall ash at ambient temperatures has little effect on standing vegetation. Shoots of evergreen conifers could be seen growing through consolidated ash even when it was compacted between needles and had remained in place for several months. Ground cover was similarly little affected except when it was completely buried under several centimetres of ash. Indeed there is some evidence from the effects on agriculture that decimation of the insect population and the supply of micronutrients actually increases yield where ash fall is light. In areas distal from a vent, ash-fall alone is unlikely to bring about substantial vegetational disturbance or changes in community composition unless ashfall is great and/or repeated at great frequency (several times a growing season for several consecutive years). The concentration of organic debris within air-fall ash (as distinct from blast deposits) in areas proximal to MSH was in most part very low (Waitt and Dzurisin, 1981) (Fig. 37). Presumably this was because the energy of the lateral blast transported the debris to more distal regions. Ash layers within alpine lakes in the Pacific Northwest of North America are commonly encountered (e.g. Dunwiddie, 1986) and may play a role in the preservation of lake-bottom organics. Not all ash falls dry. The thermal and convective energy together with water vapour released by an eruption frequently produce intense rainstorms, and as ash particles fall through the wet atmosphere they accrete into spherical lapilli. The grain size, chemistry and atmospheric conditions all combine to form a variety of ash-fall deposits that preserve various elements of vegetation in different ways. This aspect of taphonomy is little studied as yet but the following example shows the type of information that might be recovered.

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SANDV SILT, LAPILLI

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PCCRETlONARi LAPlLLl UNIT

FINE SAND MEDIUM SAND COARSE SAND

BLAS

SMALL- PEBBLE GRAVEL, SANDV MATRIX

DEPOSI1

SURGE UNIT

PEBBLE GRAVEL, SAND, SCATTERED WOOD

WOOD AND/OR REGOLITH

REWORKED BASAL UNIT

S O I L / FOREST FLOOR

Fig. 37. Composite section of blast and air-fall deposits at MSH.

At El Chichon the multiple eruptions produced a sequence of deposits that contain considerable information about the structure of the standing vegetation. In 1984, Burnham and Spicer (1986) excavated a series of I-m2 plots at various distances from the crater, and noted the occurrence and nature of plant remains in the context of the 1982 ash stratigraphy. Areas where all the vegetation was killed were studied as well as areas in which the vegetation received only a few centimetres of ash fall. A typical section is shown in Fig. 38. All the ash sequences rest upon the pre-eruption soil horizon, and the initial upward-fining pyroclastic deposits produced by the initial (28 March) eruption (approximately equivalent to the A1 airfall deposits of Sigurdson et al., ( 1 984)) preserved the autochthonous forest-floor litter together with the remains of ground-cover plants. Even relatively delicate elements such as Selaginella spp. were preserved. This unit was often capped by a crystalline tuff which in turn was overlain by very fine ash deposits in which leaves of Theobroma were preserved both as compressed intact material and as finely detailed impressions. Typically, the fine ash coated both leaf surfaces, and the early formation of impressions means that even if all the organic material eventually decayed, a record of the leaves would still exist. This layer (equivalent to the Sigurdsson et al. (1984) A2 ash of the 3 April eruption) was barren in areas that were not planted with Theobroma. Overlying this ash layer were varying amounts (depending on proximity and exposure to the vent) of ash and pumice, together with occasional organic fragments and airfall lapilli. These were interpreted to be the result of the final phase of eruptive activity. The basal litter layer reflected the herbaceous ground cover, the subcanopy, the canopy and occasional epiphytes. Although flowers were rare,

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Fig. 38. Section through air-fall deposits produced by the 1982 eruptions of El Chichon. a. pre-eruption soil horizon; b, preserved pre-eruption litter and ground cover vegetation; c. fining upward air-fall ash produced by the eruption on 28 March; d, crystalline tuff; e. fine ash with leaf impressions of Theobroma abscised as the result of ash-induced light attenuation on 28 March and air fall from eruption on 3 April; g, ash from the final phase of eruptive activity; h. recovery vegetation. Thickness of the sequence is variable, but typically not more than 1.0 m (based on Burnham and Spicer, 1986).

fruits and seeds were frequently encountered. The second plant layer, which almost exclusively consisted of Theobroma leaves (Fig. 39a), was interpreted to have resulted from predisposition to abscission induced by light attenuation from ash produced by the initial eruption. Leaf fall occurred under the weight of wet ash deposited on 3 April. Successive eruptions over a short period of time can therefore produce sequences of overlying plant assemblages that represent vertical structure within the vegetation and not, as one might assume, changes in vegetation with time. Scattered throughout the air-fall ash and surge deposits at El Chichon were isolated charcolified or scorched plant fragments. Exposure to high temperatures, even briefly and before charcoalification can take place, effectively sterilizes the plant material, and this, together with rapid burial, enhances the preservation potential. D. LATERAL LAKES I N VOLCANIC TERRAINS

Mud and debris flows initially choke drainage systems that radiate out from vents. As the flows pass the mouths of tributary valleys, volcaniclastic dams are formed. These dams, some of which in the case of MSH were over 40 m high, cause ponding of tributary streams and as a result a series of lateral

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Fig. 39. (a) Impressions of Theobroma leaves in air-fall ash from the eruption of El Chichbn on 3 April (layers e in Fig. 38); (b) colonization of ash surfaces by climbers at El Chichbn in March 1982. Climbers in the sub-canopy environments survived at the margins of the surge devastated areas whereas canopy trees were killed by the hot convectively rising surge cloud.

lakes form (Figs 27, 30b, 40a,b). The size and longevity of a lake depends on the size of valley dammed, the height and mechanical properties of the dam, and the rate of sediment input into the lakes. Stream inflow eventually leads to overtopping of the debris dam and erosion of the dam itself. The degree of erosion will depend on the mechanical properties of the dam, and although many lakes will be entirely drained, many will not. The pre-1980 Spirit Lake was an example of a “permanent” lateral lake formed by an earlier eruption,

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Fig. 40. (a) A large delta fan developing in Coldwater lake in August 1984-MSH is in the distance; (b) log debris in south Coldwater valley in August 1980. Similar log jams existed in Coldwater lake before they were recovered for timber, and would normally form a major component of basal post-eruption lake deposits.

and the sediments of Spirit Lake are likely to contain a detailed record of multiple phases of vegetation destruction and recovery. Streams flowing in to these lakes rework unconsolidated volcaniclasts, together with the remains of the pre-eruption vegetation (including large logs (Fig. 40b)), into the newly-formed lakes, and fluvio-lacustrine deltas quickly develop (Fig. 40a). At El Chichhn, lateral lakes formed along the side of the Rio Magdalena valley (Fig. 32b) but were drowned by the ponded river. The

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deltas continued to build out into the newly formed Rio Magdelena Lake and when it drained they were exposed for study (Fig. 16b). Observations on these deltas showed that initially the rate of volcaniclastic input is high and plant debris may be present only in very low concentrations. Nevertheless, as weathering forms surface crusts on the exposed ash and drainage systems reestablish themselves, the rate of inorganic sediment supply is likely to fall, grain size will decrease, and the concentration and preservation potential of litter derived from recovery vegetation is likely to increase. As plants recolonize the devastated area, their litter (including pollen) becomes incorporated into the sediments in a similar manner to that already described for non-volcanic settings. Because of the relatively rapid sedimentation rates and the progressive nature of their development, fluviolacustrine deltas in post-eruption lateral lakes potentially provide a detailed record of spatial and temporal relationships of plants during the vegetation recovery. The lake sediments themselves are likely to overlie air-fall volcaniclastics and/or mud and debris flow material containing the remains of pre-eruption vegetation, and this in turn may overlie pre-eruption soil and litter horizons. The lake sediments will mostly be finely stratified fine-grained volcaniclastics blown or washed in from the surrounding valley slopes. Immediately following the initial 1980 eruption the trophic structure of existing lakes in the MSH area was profoundly altered and many appeared to be dominated by micro-organisms typical of anoxic waters (Larsen and Geiger, 1982; Wissmar et al., 1982). Spirit Lake, for example, suffered a 22fold increase in alkalinity, enriched metal concentrations, and an increase in phenolic compounds derived from leaching and partial pyrolysis of organic debris. In spite of the profound limnological disorder, Larsen and Geiger ( 1 982) found I3 species of diatoms in Spirit Lake during August 1980, indicating that recovery was underway. The post-eruption chemistry of all the lakes in the MSH area depended strongly on their positions relative to blast trajectory, ash falls, lahars and pyroclastic flows. By 1984 abundant silica supply and nutrients derived from the weathering of fresh ash had produced eutrophic conditions, and abundant diatom and chrysophyte populations reflected individual lake chemistries (Smith and White, 1985). In Spirit Lake high sodium concentrations were associated with the occurrence of Cyclotella meneghiniana Kutzing, a diatom normally found in slightly saline waters. Fungi typical of those saprophytic on decaying wood were also found in abundance. Diatom frustules and, to a lesser extent, chrysophyte statocysts, often comprise a major portion of lake sediments and may lead to equisite preservation of terrestrially-derived plant litter. Moreover, the composition of the diatom and chrysophyte populations reflects lake chemistries which, as Ferguson (1985) pointed out, play an important role in determining speciesdependent relative degradation rates in leaf litter.

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The post-eruption high rates of sedimentation and abundant supply of mineralizing fluids within volcanic terrains provide the potential for recording in detail vegetation changes associated with severe ecological disturbance. The massive disruption of vegetation proximal to an explosive volcanic event means that large quantities of diverse plant organs are introduced rapidly into sedimentary environments, often with their preservation potential enhanced by heat treatment. Although the energy of the eruption in many cases obscures the evidence for connection between organs by widely distributing parts of the same plant, the burial of pre-eruption soil and litter horizons by air-fall ash, or pyroclastic flows and surges, preserves autochthonous associations and even more or less whole plants. The suite of assemblages produced during eruptive events therefore may provide a good overall sample of the community mosaic as it existed at the time of the eruption. It follows from this, however, that in order to reconstruct the pre-eruption vegetation in any reliable way, several contemporaneous deposits must be examined, and their positions relative to the vent must be determined as accurately as possible. Vegetation preserved during an eruption may or may not be in a climax state. Periodic eruptions disturb communities to a greater or lesser degree (depending on the nature of the vegetation, aspect in relation to the dynamics of the eruption, distance from the vent, etc.), and reset seral development to an earlier stage in the succession or disrupt normal seral stages by selectively removing component taxa. Volcanic disturbance, although similar to disturbance, say, on a “normal” floodplain, often has unique characteristics because, for example, edaphic conditions are changed with altered drainage and chemistry. Nevertheless, assemblages preserved in volcanic terrains can provide data critical to understanding ancient vegetation dynamics. A significant body of literature exists on post-eruption vegetation recovery (e.g. Adams and Adams, 1981; Spicer et al., 1985; Eggler, 1948, 1959, 1963; Halpern and Harman, 1983; Hendrix, 1981; Gadow, 1930; Smathers and Mueller-Dombois, 1974; Manko, 1975), but few studies have been carried out on plant succession in relation to the potential fossil record. As an example of patterns of regeneration that are likely to have different palaeobotanical signals, I shall consider events at MSH and El Chichon and speculate on their possible fossil records. The mixed coniferous forest that formed much of the pre-1980 vegetation in the MSH area had suffered no volcanic disturbance since the eruptions of 1857, and even then the only regions severely affected by those eruptions were probably within 5 km of the vent. Although some logging operations had been carried out, much of the area around Spirit Lake was protected to a degree from logging within the Gifford Pinchot National Forest. Aspects of

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the vegetation are documented in Adams and Adams (1981) and Saint John (1 976). In addition, extensive aerial photograph coverage exists. Recovery within the blast area has depended to a large extent on the degree of disturbance suffered and the thickness of sediments deposited. Within a few months of the 1980 eruption, isolated wind-dispersed angiosperm species, notably composites, had begun to grow even on deep pyroclastics within a few kilometres of the crater. However, the most abundant higher plant, at least in terms of area covered, colonizing exposed ash fields and valley bottoms, was Equisetum regenerating from fragmented and blasttransported rhizomes. In my experience gametophytes and young sporophytes were absent. Ferns were rare and isolated. On slopes where the soil remained in place but covered by only several centimetres of ash, typical understorey and post-disturbance (fire/logging) taxa grew in abundance (e.g. Epilohium, Equisetum, Cirsium and a few grasses). By 1982 these slopes also supported 2-3-m high bushes of several species of Rubus (salmonberry, blackberry) and Sambucus. On the North Toutle valley debris flow, several more or less permanent ponds formed and within 2 years had begun to support marginal communities of Typha. Carex and Juncus. In places, large pieces (2-3-m diameter) of blast- and flow-transported pre-eruption forest floor could be seen supporting diverse communities that had regenerated from the contained seed and rhizome bank (Fig. 34b), and thus acted as inocula. By 1984 large areas of the flow were being colonized by Lupinus. Towards the margins of the blast zone in the Green River valley, mature riparian Platanus trees survived blast and heat-kill largely because at the time of eruption they were still in bud. The leafless branches offered little obstruction to the blast and therefore remained largely undamaged, while bud scales limited heat damage to the young leaves. Similarly, understorey angiosperms, including climbers, fared better than the canopy-forming conifers. Recovery studies lower in the Toutle drainage have been hampered by artificial reseeding with grass and Alnus, but it is clear that the initial phases of recovery would naturally be dominated by Equisetum (by rhizome regeneration) by a variety of angiosperms from in situ or wind-transported seeds, and by fortuitous survival because of the seasonal timing of the eruption. In contrast to the several metres of growth exhibited by some woody angiosperm taxa, naturally regenerating conifers were only several centimetres high by 1984. Clearly, for some time to come naturally regenerated vegetation would be likely to be dominated by angiosperms and mark a complete change from the climax conifer forest. Although angiosperm taxa are more diverse in marginal aquatic (and therefore depositional environmental) settings, in the regional coniferous forest of the Pacific Northwest conifers are well represented in depositional environments not intimately associated with vulcanism (e.g. Dunwiddie, 1987) and would be expected to form a significant proportion of both pollen

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and megafossil assemblages derived from climax vegetation. The relative absence of conifers from the early successional stages of post-eruption recovery, however, is likely to give rise to fossil assemblages in which conifers are absent in the megafossil record (except for reworked eruption-emplaced debris) and variously represented in the pollen record. Quite clearly, both pollen and megafossil assemblages must be investigated together. This pattern of recovery also serves as a warning against naively interpreting angiosperm-rich fossil assemblages in volcaniclastics in terms of regional vegetation and palaeoclimate. Vegetation only gives a clear palaeoclimatic signal when it is in equilibrium with the physical environment; a condition most closely approached in the climax condition. It is now clear that assemblages in volcaniclastic sediments must be assumed to represent vegetation that has suffered some degree of disturbance, albeit possibly minor in the case of thin ash horizons in otherwise “normal” sediments. To my knowledge the only cases where this has been expressly recognized are in the studies of the neogene floras of the Pacific Northwest by Taggart and Cross (1980) and Cross and Taggart (1982). Post-eruption recovery studies at El Chichon offer different insights into bias in the fossil record, particularly as regards the effect of climate and the biology of available recovery taxa. The natural climax vegetation around El Chichon consists of angiosperm-dominated paratropical rainforest. Here species diversity is high, the structure of the forest is complex, and in addition to angiosperms a variety of pteridophytes form components of ground and epiphytic cover. Two years after the 1982 eruptions the primary colonizer in severely devastated areas was the fern Pityrogramma calamelanos L. (Link) (Spicer et al., 1985). In contrast to Equisetum at MSH, young sporophytes of Pityrogramma were observed in large numbers even on well-drained pumice fields on the volcano flanks, and in crevasses within 200 km of the crater rim. The most mature sporophytes were those regenerating from ash-buried rhizomes exhumed at the bottom of erosional gulleys (Fig. 36a). Spore dispersal by wind, constant high rainfall ( > 200 cm per year) and relative humidity, allowed gametophyte survival even on well-drained substrates. At the margins of the surge-devastated zone (approximately 6 km from the vent), and closer to the vent along protected valleys, canopy trees were killed but understory elements, particularly climbers, survived and proliferated. Two years after the eruptions, climbers were observed covering and encroaching on the bare ash surface (Fig. 39b). The over-representation of climbers presents a potential problem in the fossil record in that leaves of climbing plants are considered particularly useful in palaeoclimate reconstructions (Wolfe, 1978). Nevertheless, knowing that over-representation occurs goes a long way towards solving the problem. Because preferential climber survival is unlikely to occur to the same

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extent in vegetation disturbed by other agencies, differentiating volcanic disturbance from, for example, that caused by fire, is essential. Where ash fall was relatively thin, woody angiosperms had regenerated either from seed or rootstocks and grown to a height of over 4 m. This rapid regeneration of a wide variety of taxa reflects both the diversity of the original vegetation and the 12-month growing season. By way of contrast, the growing season at MSH is barely 4 months long for many taxa, and correspondingly recovery is much slower. The diversity of angiosperms at El Chichon provided a rich pool of taxa from which a variety of early colonizers could be drawn. Such diversity is not present in the climax vegetation of the MSH area. The main reason for the strong differences between the patterns of recovery at MSH and El Chichon appears to lie in the contrasting biologies present in the taxa of the pre-eruption vegetation. Conifers suffered more damage and were slower to recover than the angiosperms; a situation likely to persist for some time in view of the longer gymnosperm life cycle. If such profound differences in recovery patterns can be seen in just these two contemporaneous examples (and here I have given only the briefest of accounts), the potential for studying even more exotic dynamics in ancient vegetation under radically different climates and composed of extinct taxa, is very exciting. Armed with just some of the insights into assemblage formation in volcanic terrains that studies of this kind provide, major new contributions to ecology and evolutionary studies are possible. The fossil record, with its extended time-scale, offers a unique perspective on this aspect of biology.

XI. PRESERVATION A N D DIAGENESIS The post-burial chemical and physical changes that determine whether or not a plant part will be preserved, and the quality of that preservation, are varied and, as yet, poorly understood. The most common modes of preservation may be categorized for convenience into compression/impressions, duripartic (hard-part) preservation, permineralizations and petrifactions, and casts and moulds (Schopf, 1975), although these categories are not mutually exclusive. A. COMPRESSlON/IMPRESSIONS

In some instances plant material may become coated with a mineral layer (often iron hydroxide/oxide) in aquatic regimes prior to burial (Spicer, 1977). This phenomenon is most noticeable in post-eruption volcanic terrains, because weathering of fresh ash releases large quantities of iron into stream water. Preferential preservation of plant assemblages in iron claystone

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nodules in bentonites yields high-quality impressions (Spicer and Parrish, 1986). The pre-burial formation of mineral coatings not only protects the plant part from abrasion but it may also deter invertebrate feeders. Once buried, plant material is subject to the compaction processes that occur within the sediment as a result of dewatering and loading by addition of new sediment. Decay of cell contents usually takes place within a few days of death or entry into an aquatic environment, and if air is not excluded, cellulose is also rapidly destroyed, even in woody tissue (Rolfe and Brett, 1969). Herbaceous material therefore has to either form a competent impression template, be mineralized, or enter into an anaerobic or disaerobic environment very rapidly in order to be preserved. If early mineralization does not occur and provide support, sediment loading causes the tissues to compress as cell walls collapse. Walton (1936) proposed that in the compaction process there is very little lateral expansion of tissues and distortion is mostly in the vertical plane. This has been largely confirmed by recent experiments (Rex, 1983, 1986; Rex and Chaloner, 1983), but because of internal tissue complexes and resistant surface features on opposing surfaces, the final topography of the compression fossil and its matching impression can be complex, lead to serious misinterpretations of biology, and thus incur taxonomic confusion. B. DURIPARTIC PRESERVATION

The inert qualities of sporopollenin impart a very high preservation potential to pollen and spores which, consequently, are the most abundant evidence of past plant life. However, other plant substances such as cutin and lignin are also highly resistant to decay. When plant material is heated in the total or partial absence of oxygen, volatile compounds are driven off, and if the process is continued to completion, the result is charcoal (fusain) composed entirely of inert carbon. The charcoalification process typically leads to some shrinkage of the tissues but anatomical detail is preserved (Harris 1958; Alvin et al., 1981). Thus charcoalification either by natural fires or by pyroclastic burial during volcanic activity greatly enhance the preservation potential of plant material and produce fossils yielding levels of botanical information which rival those seen in permineralized specimens. C. TISSUE MINERALIZATION

Plant fossils with the greatest amount of botanical information are those preserved anatomically in three dimensions. Apart from charcoalification, this is brought about by early impregnation of tissues by minerals. Plants are most commonly preserved by various forms of silica (chert, opal), calcium/magne-

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sium carbonate, and pyrite, all of which can preserve individual specimens in clastic environments or occur within fossil peats (Scott and Rex, 1985). In many instances organic cell walls remain after the cellular spaces have been filled with minerals. Such specimens are referred to as being permineralized. Where the organic material has been subsequently replaced by mineral matter (either the same as that infilling the cellular spaces or different), the specimen is referred to as a petrifaction. The processes of mineralization can be complex. Although silicification has been thought of as a process of deposition of silica onto cell wall surfaces (Drum, 1968),or organic replacement on a molecule by molecule basis (Correns, 1950; Iler, 1955), the current preferred model is one of infiltration (Schopf, 1975; Leo and Barghorn, 1976; Sigleo, 1978; Jefferson, 1982; Knoll, 1985). A possible model for silicification in volcaniclastics is given in Karowe and Jefferson (1987), but a comprehensive review of the topic is outside the scope of this chapter. Rates of silicification can be extremely rapid as evidenced by the preservation of cell contents (Knoll, 1985). However, in studies at Mount Saint Helens, Karowe and Jefferson (1987) showed that in woods in that particular environment, incipient silicification could be documented after 100 years burial, and that in woods buried for 36,000 years, silica impregnation of cell walls had taken place. An important consideration here is that in spite of the apparent permeability of the lahar sediments, buried wood survives in an unmineralized state long enough for this protracted process to take place. These observations explain the relatively common occurrence of “fossil forests” in volcanic terrains. The origin of carbonate nodules and sheets in coal (coal balls), in which plant material is permineralized, has been controversial for some time. This is because peat environments are generally acid, whereas alkaline conditions are necessary for the precipitation of carbonate. Preservation is variable, depending on when permineralization took place in relation to decay and compaction processes, but often exceptional detail is preserved, such as cell contents (Taylor, 1977), nuclei (Millay and Eggert, 1974), pollen drops (Rothwell, I977), and gametophytes (Brack-Haynes, 1978). By serial sectioning of populations of coal balls, ancient plants may be painstakingly reconstructed (e.g. Rothwell and Warner, 1984), or used for palaeoecological studies (e.g. Phillips et al., 1985). In spite of the palaeobotanical importance of coal balls, hypotheses concerning their formation are varied. Scott and Rex (1985) review the various explanations that have been proposed, and therefore only brief consideration will be given here. The source of carbonate is a particularly vexing problem. Stopes and Watson (1 908) proposed a marine origin and envisioned sea water permeating uncompacted peat as a result of marine transgressions. However, not all coal-ball-bearing coals are overlain by marine units. Mamay and Yochelson (1 962) suggested that breaching of beach barriers separating coal-forming

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swamps from the sea might introduce sufficient carbonate, but this would also mean that transported marine organisms would occur within some or many coal balls and that there would be massive frequent disturbance of the swamp community due to changes in groundwater salinity and pH. Such changes should be detectable in the palynological record if not in that of the megafossils. Coal balls with marine organisms at their core are common, but are not universally found. Infiltration of the peat by non-marine carbonate-rich groundwater is another possibility (Feliciano, 1924; Evans and Amos, 1961; Phillips and DiMichele, 1981; Retallack, 1986), but this does not explain the marine cores of some coal balls. The diverse nature of coal balls means that all the above hypotheses are valid, but not universally. The variety of coal-forming environments also suggests that no single model accounts appropriately for coal-ball formation. However, another scenario, not considered by Scott and Rex (1985), is also possible and could be taphonomically investigated in modern environments. The recognition that many commercial (thick) coals may originally have been ombrogenous (raised) mires would tend to disfavour both the barrierbreach model and groundwater model, particularly for the upper parts of the seams. However, modern raised mires are known to occur on fluvio-marine deltas. As peat accumulation takes place, subsidence is also occurring and the basal parts of the peat may sink below the base of the non-marine groundwater lens into saline groundwater of marine origin. Thus any given portion of the peat will initially form in an acid environment and subside into an alkaline, carbonate-rich environment, without the living mire vegetation experiencing any effects. The relative rates of peat formation and subsidence will control the thickness of peat immersed in the carbonate source, and the degree of compaction that takes place prior to mineralization. If subsidence outstrips mire growth all the peat could be exposed to marine influence, either by immersion in saline groundwater (equivalent to the transgression model), or storm breaching, or both. Pyritization of plant material is common and can preserve fine detail (e.g. Wilkinson, 1984) and clearly can happen very early in the diagenetic history of buried plant matter. It often occurs in marine environments where sulphur, iron, and reducing situations occur together, but as these ingredients are also present in non-marine settings, particularly where organic matter is accumulating, pyritization itself is not diagnostic of any particular depositional environment. D. CASTS AND MOULDS

The infilling of plant cavities with sediment, either before or after some decay has taken place, has the potential to give rise to a three-dimensional cast of

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the cavity morphology which may or may not have been partially compressed prior to sediment hardening. The cavity left in consolidated sediment after decay of a plant part yields a mould that subsequently may be filled either by sediment or mineral growth (or both) to give a cast. Only gross morphological features are preserved and great care is required in interpreting which surface is replicated, and whether that surface is a true indication of the life condition instead of an artefact of decay. Rex (1985) investigated experimentally the infilling of hollow stems and showed that grain size sorting and progressive infilling within such cavities, apart from being dependent on all the usual sedimentological criteria such flow velocity, grain size mix, and orientation of the cavity with respect to flow, can lead to differential compaction and distortion of plant tissues. However, this distortion, although compounding the difficulties of biological interpretation, can also be extremely useful in documenting depositional history and therefore has considerable palaeoecological significance.

XII. APPLICATIONS OF PLANT TAPHONOMY TO THE FOSSIL RECORD The need to understand fossilization processes as an aid to interpreting individual fossils or assemblages has long been recognized. Indeed, the first quantitative taphonomic study was undertaken as long ago as 1924 in order to understand better both the vegetational composition and climate represented by a fossil assemblage (Chaney, 1924). This was closely followed by Walton’s (1936) pioneering work on compressional deformation. In spite of these and other taphonomic exercises, most taphonomic work has been undertaken during the last twenty years or so. The impact of taphonomy on palaeobotany in general is only just being felt. As a crude measure of this impact it is interesting to note that at the 1980 International Organization of Palaeobotany Conference most papers concentrated purely on the botanical aspects of plant fossils, whereas by the 1984 meeting very few papers failed to discuss to some degree the sedimentological environment of individual fossils or assemblages. The applications of plant taphonomy to interpretations of the fossil record are scattered throughout the literature, and while no single palaeobotanical study has been “revolutionized” by taphonomy, many studies have benefited in some way from it. This impact is perhaps best demonstrated by selecting a few studies that reflect the spectrum of scales at which taphonomy can be useful, ranging from an understanding of the conditions of fossilization of individual specimens to interpretations of regional vegetation and climate. These examples have been chosen because they have incorporated references to researched taphonomic principles rather than relying on interpretation based on speculation.

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The work of Rex (1983, 1985, 1986) and Rex and Chaloner (1983) follows from the work of Walton (1936) in trying to understand the processes that give rise to compression fossils. Here experiments have led directly to a reevaluation of the morphology, and therefore taxonomic treatment, of Carboniferous lepidodendrid leaves (Rex, 1983) and glossopterid fructifications (Rex, 1986). In the case of the compression fossil known as Cyperites, compression artefacts, and their influence on the fracture plane of the fossil during its exposure, gave rise to several forms of compression fossils that were very different to the morphology of the leaf in life. By combining the experimental compression of leaf models based on uncompressed permineralized material with observations of compressed leaves of Cyperites sectioned vertically, it was possible to redefine the genus and demonstrate that at least two fundamentally different types of leaves were borne by the lepidodendrids. In the case of the ovulate glossopterid fructifications, similar combinations of experiments and observations of fossils preserved in different ways have shown that permineralized forms represent different taxa to those represented by compression fossils (Rex, 1986). In addition, of the many models suggested for the life morphology of such fossils, only one (the seed-bearing strobilus of Walton (1936)) seems appropriate to explain the features observed in the impressions. Nevertheless, no single uncompressed structure can explain all the observed variations. It follows from this that glossopterids with fructifications of the Scutum type were more diverse than traditionally envisaged. 8. COMMUNITY RECONSTRUCTION

One of the most exciting reconstructions of an ancient community that has been made recently on sound taphonomic principles is that by Gastaldo (1987b), who studied a Carboniferous clastic swamp environment. Mining operations in Alabama exposed extensive bedding surfaces, allowing detailed assemblage analysis to be carried out along a transect from the levee-bound swamp to a channel back-levee margin. In situ tree bases of Lepidophloios, Lepidodendron and Sigillaria were preserved as casts overwhelmed by, and embedded in, 3-m thick crevasse splay deposits. The crevasse splay also capped and sealed the swamp sediments. Litter beds within the splay deposits were also sampled. Interpretation of the sedimentary system was based on analogous Holocene crevasse splay systems (e.g. Gastaldo et al., 1987). Preserved in situ tree bases and preserved swamp litter show that Lepidophloios was the tree most tolerant of waterlogging and comprised almost pure stands in the deep swamp away from the channel. Closer to the channel, where the levee pro-

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vided a degree of topographic relief (and therefore drainage), Lepidophloios was gradationally replaced by Sigillaria. Understorey vegetation increased the diversity. Closer to the crevasse splay breach, remains of calamites and pteridosperm elements increased in abundance while lycophytes were represented only by isolated leaves and rare strobili. Medullosan seed ferns were represented by large ( > 1 m) frond fragments. Whole lyginopterid fronds were found attached to metres of coiled stem, suggesting a Lane habit. Entire crowns of arborescent pteridophytes were also found. The lack of mechanical degradation and the association of fronds and stems suggests that this assemblage was transported minimally prior to burial, and represents the near channel understorey and/or riparian vegetation (cf. Fig. 6) flushed into the swamp by the crevasse. Proximal to the breach itself, the compression flora consisted of fragmented pteridosperm pinnules and pinnae together with numerous Calamites pith casts. In addition to the buried tree bases, prostrate logs, forest-floor litter, and in-washed debris, other litter horizons were interpreted to have been produced by death and crown break-up of the standing lycophytes. Death and crown break-up were probably not simultaneous, however, as two distinct litter horizons are present. This appears somewhat analogous to the sequence of leaf beds produced by volcanic air-fall ash (Burnham and Spicer, 1986). The distribution and degradation patterns of plant debris seen in this Carboniferous crevasse splay system are without doubt similar to that observed in modern sedimentological analogues. This study, in which virtually no biological analogues were invoked, confirms that the plant diversity distribution and structure in Carboniferous swamps was similar to its modern counterpart, in spite of the total dissimilarity of component taxa.

C. RECONSTRUCTING COMMUNITY SUITES AND REGIONAL VEGETATION

The luxury of having extensive bedding surfaces available for study is rare, particularly in natural exposures. Often the extent of an outcrop is insufficient for detailed characterizations of sedimentary environments, and mapping of within-community taxon relationships is impossible. Nevertheless, reconstructions of suites of communities based on detailed facies analysis in sections can be carried out successfully. For example, Cuneo (1983, 1987), working in Argentina, has recognized several communities in a Permian deltaic system. Swamps were dominated by sphenophytes, while slightly higher ground was occupied by two associations; one was composed of glossopterids, ferns and progymnosperms, while the other was composed primarily of ferns and conifers. Glossopterids and conifers occupied the driest floodplain sites (Cuneo, 1987). These kinds of study can be extended to characterize regional vegetation in

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terms of within-community taxon associations and temporal changes in community mosaics. On the North Slope of Alaska, logistic constraints and natural exposures precluded the type of work undertaken by Gastaldo (1987b); nevertheless, by examining a wide range of sedimentary facies over a wide area, the Cretaceous arctic vegetation has been characterized at the community level (Spicer and Parrish, 1986; Spicer, 1987). The pre-angiosperm late Early Cretaceous vegetation of the Corwin Delta complex of the North Slope, Alaska, consisted of riparian and overbank communities in which Podozamites and Ginkgo trees dominated, with Sphenobaiera as a subordinate component somewhat removed from the river margin (Spicer, 1987). Evidence for this is the ubiquitous occurrence of leaf and shoot litter belonging to these taxa in overbank and channel deposits. The conifers Arthrotaxopsis and Elatocladus were also present. Understorey components consisted primarily of ferns (e.g. Onychiopsis, Sphenopteris and Birisia) and sphenophytes (Equisetites)which are commonly preserved as large frond segments (ferns) or upright infilled axes (Equisetites)in overbank muds. Coal-forming mire communities were probably dominated by conifers (Podozamites is the only foliage form found associated with the coals, and tree bases and prostrate logs have been observed), but these communities were probably of low diversity. Equisetites rhizome systems were consistently found in the palaeosols beneath coals, and were clearly primary colonizers in many situations. Lacustrine margins supported a variety of plants, with taxodiaceous conifers and ginkgophytes predominating. Cycadophytes were limited in diversity compared to lower latitudes. The deciduous Nifssonia is found in near-coastal environments (Nilssonia decursiva), or in shales associated with coals ( N . alaskana). Cycadophytes with finely serrated leaf margins occupied lakeside environments. From spore evidence, lycophytes were also present. Angiosperms first arrived in the North Slope deltaic systems in latest Albian times, and the first angiosperm-rich communities were those along river margins. Plants with leaves belonging to the “platanoid” complex (Pseudoprotophyllum, Pseudoaspidiophyllum, Crednaria and “Platanus”) replaced the riparian Podozamites and ginkgophytes. Although generally supposed to be riparian “weed trees”, the stature of the platanoid leaf producers remains unknown, in that vesseled wood does not occur on the North Slope until the Paleocene (Spicer and Parrish, 1989). By the late Cenomanian, riparian communities were dominated by platanoids, but with a variety of lobed and pinnately veined entire-margined leaves in overbank, lacustrine and interfluve “pond” sediments. The ubiquitous occurrence of taxodiaceous conifer shoots in all facies suggests that in spite of the angiosperm diversity, the regional aspect of the vegetation was coniferous. Angiosperms, cyadophytes, ferns and sphenophytes were subcanopy elements (Spicer, 1987). Deliberate sampling of as wide a range of sedimentary facies as possible allowed taphonomic biases (e.g. over-

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representation of riparian vegetation) to be compensated for (Burnham, 1989) (albeit subjectively), and the physiognomy of the regional vegetation was used as part of an interpretation of the near-polar palaeoclimate (Spicer and Parrish, 1986; Parrish and Spicer, 1988). Taphonomy also played an important role in identifying the deciduous nature of the vegetation. No matter what sedimentological facies were examined, the leaf litter always showed minimal signs of degradation. This was taken to suggest that leaf abscision was synchronous across a wide variety of taxa, and all elements were incorporated into the sediments in a fresh state (Spicer and Parrish, 1986; Spicer, 1987).

D. THE USE OF PLANT FOSSILS IN SEDIMENTOLOGY

Throughout this chapter the structure and composition of inorganic sediment has been used as an aid in interpreting individual plant fossils or assemblages. However, the plant debris is also part of the sedimentary system, and, because its source and hydrodynamic properties are so different to those of the inorganic clasts, it provides important data for improved interpretations of some sedimentary processes and environments. Wnuk and Pfefferkorn’s (1987) study of a Carboniferous swamp compared the observed distributions and orientations of fossil lycopod logs (and other plant debris) with those observed in modern depositional environments. Their sedimentary sequence began with an underclay representing an accretionary floodplain soil which incorporated litter derived from the surrounding lycopod-pteridosperm forest. Episodic flooding built up a succession of horizons, but ordinarily, after the floodwaters receded, root bioturbation tended to destroy the potential assemblages. However, this sequence was terminated by a 5-cm layer of underclay in which plant debris was preserved, suggesting that a final flood event permanently drowned the forest and formed a floodplain lake. Death of the trees followed and crown break-up contributed plant material to the lake sediments. Of particular interest was the unidirectional orientation of lycopod logs in contrast to a random orientation of pteridosperm stems. No known waterrelated process could be invoked to explain the anomalous orientations of the plant parts, particularly as the assemblage was entombed in fine-grained non-volcaniclastic sediment, indicating low-energy deposition. The only model capable of explaining all palaeobotanical and sedimentological features was storm-toppling of the standing lycopods, which fell onto remains of the understorey pteridosperms. Taken in isolation, neither the inorganic sediment record, nor the plant fossil remains, could have been used to interpret the sequence of events that produced the observed sedimentary package.

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XIII. CONCLUSIONS Plant taphonomy is in its infancy, but it is a rapidly expanding field. The complexity of this multidisciplinary subject may give the impression that the diverse processes of assemblage formation prevent proper understanding of ancient plant ecosystems. This attitude is erroneous, but it should be apparent that taphonomy is a double-edged sword. On the one hand taphonomic studies expose inappropriate methodologies, analyses and interpretations, but on the other hand new sampling strategies, techniques of analysis and interpretative methodologies are emerging that allow reconstructions of ancient communities and environments at scales of temporal and spatial resolution previously not thought possible. The infancy of the subject precludes at this time the presentation of an extensive catalogue of examples where taphonomic models have contributed significantly to fossil assemblage interpretation. Nor would such a catalogue be necessarily indicative of the subject’s maturity. No single taphonomic “model” is going to be directly applicable even to a “class” of fossil assemblages, and this “package application” attitude is to be discouraged because it leads to simplistic and potentially inaccurate interpretations. For similar reasons, Miall (1985) criticizes end-member facies model comparison in sedimentological studies of inorganic particles. However, awareness of taphonomic biases is contributing to the interpretation of preservation states, systematics, community reconstructions, palaeoenvironmental studies, and palaeobiogeographic data selection (e.g. Raymond et al., 1985). It is perhaps significant that many examples of the applications of taphonomy to the fossil record have been the result of work undertaken by palaeobotanists with taphonomic experience. Taphonomic studies instil an observational approach in the researcher that forces a closer scrutiny and appreciation of the relationship between organic and inorganic sediments. Attitude and technique are more important than the application of whole models. Models are useful in that they underscore the interaction of processes to give a reasonably consistent sedimentological pattern, but they represent “landmarks” in a continuum of interactions rather than the outcome of an “either/or” process. Traditionally discarded or overlooked fragmental material contains an important taphonomic signal that is essential to our understanding of temporal and spatial relationships within source vegetation. This signal can also help our understanding of sedimentation processes. Putting plant debris in a sedimentological context therefore provides an additional class of sedimentary particles with unique properties. Through enhanced resolution at the community level, palaeoclimate reconstructions are also improved. Indeed, it is clear that corrective measures often have to be taken to compensate for the fact that differential organ transport biases assemblages, and because much of the plant fossil record

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samples disturbed vegetation. Taphonomic studies are helping to identify the most reliable assemblages and sedimentary systems for palaeoclimatological work. They are also highlighting the need for regional studies where a range of depositional environments are represented and from which community heterogeneity, and therefore local bias, can be understood. Plant taphonomy provides the means by which community heterogeneity may be resolved at both the local and regional scales, and thus complements the broad regional “floral” interpretations that abound in the literature. However, taphonomic work has highlighted the need for detailed sedimentological work in conjunction with more traditional palaeobotanical studies. Unfortunately, detailed documentation of the nature, quantity and distribution of plant debris by sedimentologists is practically non-existent in the literature, and until recently it was just as rare to find palaeobotanists recording sedimentological data relevant to their fossil assemblages. This situation is now changing, but it is clear that many of the known, indeed “classical”, plant fossil assemblage sites need to be restudied and re-evaluated in the light of taphonomic research.

ACKNOWLEDGEMENTS I am grateful to the following individuals and agencies for their support of my taphonomic research: Don Peterson, Harry Glicken, and other personnel of the USGS Cascades Volcano Observatory, The Royal Society of London, Servando de la Cruz Reyna, Paul Grant, Robyn Burnham, Peter Crane, David Ferguson, The University of London Central Research Fund, Goldsmiths’ College Research Fund, and the Natural Environment Research Council. I also thank Judith Totman Parrish, Bob Gastaldo, and an anonymous reviewer for constructive criticisms of the manuscript. The photographs in Fig. 26 (a,b) were taken by J. Stewart Lowther, and I am most grateful for permission to reproduce them here.

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Primary Productivity in the Shelf Seas of North-West Europe

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Methodsfor EstimatingPrimary Productivity . . . . . . . . A . Nutrient Budgets . . . . . . . . . . . . . . . . B. Oxygen and Carbon Fluxes . . . . . . . . . . . . C. Biomass Distributions . . . . . . . . . . . . . . D . Primary Productivity Models . . . . . . . . . . . .

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Environmental Conditions for Phytoplankton Growth in the NW European Shelf Seas . . . . . . . . . . . . . . . . . . . . 217 A . Mixing Processes, Seasonal Stratification . . . . . . . . . 217 B. Light Availability . . . . . . . . . . . . . . . 220 C . Nutrient Availability . . . . . . . . . . . . . . 223 D . Grazing . . . . . . . . . . . . . . . . . . . 225 226 E. Annual Production Cycle. . . . . . . . . . . . . .

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EvaluationofPrimary Productivity Estimates . A . General Considerations . . . . . . B. Mixed Waters . . . . . . . . . . C . Stratified Waters . . . . . . . . . D . Frontal Regions . . . . . . . . . E . Spatial and Temporal Variability . . .

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Fate of Plant Material within the Shelf Ecosystem

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I. INTRODUCTION The photosynthetic activity of phytoplankton in the surface layers of the oceans accounts for about 93% of organic carbon production in the marine ecosystem (Woodwell et al., 1978), the remainder being due to other types of plants mainly in coastal and estuarine environments. Continental shelf waters are, on average, about three times as productive as open ocean waters, so that they contribute a relatively large proportion of total marine phytoplankton productivity ( 20%) relative to their area. Reliable estimates of phytoplankton productivity are required for assessments of the biological resources of the oceans. Attempts to estimate and compare potential fish yields for particular areas (Jones, 1984; Brander and Dickson, 1984), or to predict the impact of overfishing or hypernutrification (van Bennekom et al., 1975; Ursin and Andersen, 1978) on the marine production cycle, depend on a knowledge of primary production rates and the factors that control these rates. Furthermore, it is now apparent that phytoplankton have a fundamental role in biogeochemical cycling in the oceans through direct involvement in the exchanges of material between the atmosphere, surface waters, deep waters and sediments (Whitefield, 1981). The main relationships of phytoplankton growth to ecological and biogeochemical processes in the sea are summarized in Fig. 1. In general the most useful measurement of phytoplankton productivity is net photosynthetic carbon fixation (i.e. gross photosynthesis minus respiration) per unit sea area over a period of 24 h (or some multiple of whole days). However, there are several basic problems in estimating net production which are given remarkably scant attention in the general literature on the productivity of marine phytoplankton and lead to difficulties in the evaluation of published data. These include: 1. For measurements of carbon assimilation (usually made with I4C as a tracer), uncertainties about the degree to which rates of carbon fixation in the light are representative of net photosynthetic rates (Dring and Jewson, 1982), and about rates of dark respiration (Steemann Nielsen and Hansen, 1959; Raven and Beardall, 1981; Joiris et al., 1982). 2. For oxygen measurements, uncertainties in the photosynthetic assimilation quotients used to convert rates of oxygen exchange (photosynthetic or respiratory) to equivalent carbon values (Williams et al., 1979; Megard et al., 1985). 3. For turbulent waters, uncertainties over vertical mixing coefficients that effectively determine the mean irradiance field, and therefore rates of photosynthesis (Lewis et al., 1984), as well as the depth range over which dark respiration losses must be estimated to give net production for the phytoplankton population as a whole (Sverdrup, 1953). Another important consideration is the relationship between the form of nutrient supply for phytoplankton production and the capacity of the pelagic

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Fig. 1. Phytoplankton growth in shelf seas-cological and biogeochemical processes. P, phytoplankton; H, herbivores; C, carnivores; MH, microheterotrophs; DOM, dissolved organic matter; POM, particulate organic matter; VOM, volatile organic matter; Bio, biominerals (opal, calcite). For the sake of clarity, only the more important relationships are shown.

ecosystem to support over an annual time-scale a net export of organic material to deep water, to the sediment, and as fish catches. Growth of the plant cells in surface waters is dependent on a combination of external or “new” inputs of nutrients-mainly resulting from the upward mixing of deep water, but also from terrestrial and atmospheric sources-and of internal or regenerated nutrients released during the biological turnover of material within the euphotic zone (Dugdale and Goering, 1967). The significance of this distinction was examined by Eppley and Peterson (1979), who reached two important conclusions. Firstly, it is the new production of phytoplankton, as opposed to regenerated (or total) production, that represents capacity for the export of organic material from the euphotic zone; secondly in most environments new production is a relatively small proportion (e.g. 30% for a station in the subtropical Atlantic Ocean-Platt and Harrison, 1985) of total annual primary productivity. Although some care needs to be taken in defining the scales over which new and regenerated production is estimated

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(for example, should inorganic nutrients produced by mineralization processes below the seasonal pycnocline and returned to surface waters two or more times within the same year be considered as new nutrient sources?), this general concept has proved invaluable in attempts to assess quantitatively the ecological and biogeochemical implications of phytoplankton growth (Platt and Harrison, 1985). The past two decades have also been a period of rapid progress in physiological investigations on planktonic algae, particularly in relation to the utilization of nutrients and light energy. Much of this work has been based on laboratory experiments with uni-algal cultures, mainly because of the difficulties in interpreting physiological data on heterogeneous natural phytoplankton assemblages. Although the results have added greatly to our knowledge of the various ways in which environmental conditions influence the growth and succession of phytoplankton (Harris, 1984), it has also led to a tendency to use simplified, and often inappropriate, sets of parameters for quantitative descriptions of natural populations (Talling, 1984). Thus, from an ecological standpoint, recent advances in algal physiology have not necessarily added a great deal to our knowledge about rates of primary productivity in the sea. For the NW Europe continental shelf, the generally accepted picture of primary productivity is still based largely on studies carried out more than 20 years ago (Harvey et al., 1935; Steele, 1956; Cushing, 1963). Physical mixing processes in this region are known to exert a fundamental influence on the distribution and abundance of phytoplankton species (Pingree et af.,1978) in a spatial as well as a temporal context. However, except for particular studies such as the FLEX experiment in the North Sea (Radach et al., 1982), few attempts have been made to bring together new ideas on the environment and growth of phytoplankton in a re-evaluation of data on primary productivity. The main objective of this chapter is to summarize present knowledge of phytoplankton distributions and growth in the shelf seas of NW Europe in the context of a broad understanding of phytoplankton ecology, both from experimental laboratory work and from observational studies of other ocean areas. In the sections on the control of phytoplankton production and on methods for estimating primary productivity, the references are largely to the general literature, whereas the remaining sections deal specifically with NW European waters. Such an approach leads to some repetition, but provides a more comprehensive basis for assessing primary productivity in this region.

11. ECOLOGICAL A N D PHYSIOLOGICAL PERSPECTIVES A. PHYTOPLANKTON DISTRIBUTIONS

1. Descriptive Accounts The early studies of P. T. Cleve, H. H. Gran, H. Lohmann, C. H. Ostenfeld

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and others provided much of our basic knowledge of the distributions of larger phytoplankton species in the NE Atlantic Ocean, and this is summarized in the floras of Lebour (1925, 1930) and Schiller (1933, 1937). Subsequent work has been concerned largely with the life histories of diatoms and dinoflagellates, as well as descriptions of the many naked and scalebearing marine flagellates (for references and up-to-date nomenclature see the checklists of Hartley (1986) and Parke and Dixon (1976), and also the account of Helgoland phytoplankton by Drebes (1974)). The ecology of the various flagellate groups is still relatively poorly known, with the exception of a few widespread and easily recognized species such as the prymnesiophytes Phaeocystis pouchetii and Emiliania huxleyi; the investigations by Throndsen (1976), Heimdal and Gaarder (1980, 1981) and Estep et a f .( 1984), although not confined to shelf environments, give some indication of the abundance and variety of these organisms. Furthermore, the presence in shelf waters of numerous photosynthetic prokaryotic and eukaryotic cells, < 2 pm in diameter, has become generally recognized only during the last few years (Joint and Pipe, 1984; Murphy and Haugen, 1985; Fogg, 1986). Another feature of distributional studies is reports of extensions in geographical range for certain species. For example, the large diatom Coscinodiscus waifesii (Boalch and Harbour, 1977) and the bloom-forming dinoflagellate Gyrodinium aureolum (Braarud and Heimdal, 1970) appear to be recent introductions from other parts of the world and are now wellestablished species in European shelf waters. 2. Quantitative Methods The size range of marine phytoplankton extends over at least seven orders of magnitude in terms of cell volume ( < 1 to > 10’ pm3), so that cell concentrations are not a useful measure of total biomass or of relative biomass for individual species. Two approaches are used to overcome this problem, the first based on pigment determinations generally as total chlorophyll a (Strickland and Parsons, 1972), and the second on the conversion of cell counts or chlorophyll to phytoplankton carbon (Strathmann, 1967; Banse, 1977). Although both methods are subject to several sources of potential error, they do give internally consistent measures of spatial and temporal differences in phytoplankton standing crop (Holligan et al., 1984a) as well as information on the contribution of individual taxa (e.g. accessory pigment groupings (Mantoura and Llewellyn, 1983)) or species to the total population. Statistical techniques for deriving phytoplankton carbon from measurements of particulate organic carbon, with the condition that the phytoplankton represent a variable and often minor component of the total carbon, have also been developed (Eppley et al., 1977). An ancillary method for discrete pigment determinations is the use of in vivo fluorometry (Lorenzen, 1966), which provides a continuous record of chlorophyll fluorescence as horizontal (surface) or vertical (depth) profiles

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that can be compared with those for temperature, salinity or other hydrographic properties. Great care must be taken over calibration of the fluorometer records, as fluorescence yields per unit chlorophyll can vary by up to an order of magnitude with changes in physiological state or species composition of the phytoplankton population (Pingree et al., 1982). For studies of large-scale distributional patterns of phytoplankton, use has been made of the colour (pigment) index given by tows of the Continuous Plankton Recorder (CPR) (Robinson, 1970). Some caution must be exercised in the interpretation of CPR data as the mesh size (270 pm) of the collection net will tend not only to select the largest phytoplankton cells but also vary as a result of partial clogging within dense populations. Furthermore, the monthly sampling interval for the routine CPR routes may be too infrequent to resolve some of the main features of phytoplankton succession in temperate waters. Ten years of chlorophyll measurements for March to July in the northern North Sea are compared in Fig. 2 with monthly CPR colour indices over a similar period. Detailed ship studies, such as the 1976 FLEX experiment (Radach et al., 1982), confirm that the duration of the spring diatom bloom is generally less than two weeks. Thus, in the CPR records, the absence of a spring outburst on some years (Fig. 2b) is probably not real but attributable to infrequent sampling, and the apparent decrease in the total abundance of spring phytoplankton (Reid, 1978) may reflect just a decline in numbers of large diatoms which are generally a minor component of the spring bloom. 3. Temporal and Spatial Distributions Through the many observations on species abundance, chlorophyll concentration and the CPR colour index, a consistent picture of annual changes in phytoplankton abundance has been built up. There are marked differences from one type of environment to another (e.g. Robinson et al., 1986), due mainly to the influence of vertical mixing on the availability of light energy and nutrients to the plant cells (see Section 111 for a detailed discussion). The extremes are seasonally stratified waters, which are characterized by surface chlorophyll maxima in the spring and autumn and a subsurface maximum in the summer associated with vertical nutrient gradients in the thermocline (Fig. 3; Holligan and Harbour, 1977), and well-mixed waters with just a midsummer chlorophyll peak extending through the whole water column (e.g. in the Bristol Channel (Joint and Pomroy, 1981)). However, there are still relatively few sets of observations to show the complete seasonal cycle of phytoplankton, so that the CPR data remain the best general source of information for comparing one region to another. For example, the distinction between stratified and mixed waters is well shown by the CPR data for the central North Sea and central Irish Sea respectively (Colebrook, 1979). One feature that has yet to be properly assessed by more absolute sampling methods is the autumn phytoplankton maximum. As

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Fig. 2. Comparison of surface chlorophyll a measurements, 1961-1970 (from Steele and Henderson, 1977) (a) and the CPR pigment index, 1958-1973 (from Reid, 1977) (b) for the northern North Sea. For any particular year the spring bloom, defined as chlorophyll values > 2 mg m -3, appears to last about two weeks (e.g. Radach et al., 1982). The relative chlorophyll levels represented by the contours of CPR pigments are approximately 1.0 : 1.6 : 3.4.

pointed out by Steele (1956), rates of production are very variable at this time of year, and results from the CPR indicate that this is particularly true for regions of intermediate seasonal stratification such as the central North Sea (Reid, 1978). A complementary approach to studies on temporal distributional patterns

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Fig. 3. Annual chlorophyll a (mg m I) distribution at station El in the western English Channel based on two years observation (1975-1976). Adapted from Holligan and Harbour (1977). who give details of sampling methods.

is to consider spatial (horizontal) changes in phytoplankton biomass. A detailed study of this type was carried out by Pingree et al. (1975), who related differences in phytoplankton abundance and species composition to hydrographic properties on a section across a tidal front in the western English Channel. The results showed not only the clear difference between well-mixed and well-stratified waters during the summer, but also the enhanced biological activity in association with the transitional frontal boundary (Fig. 4). The characteristic time- and space-scales of changes in chlorophyll concentrations (Figs 3 and 4) demonstrate the difficulty of adequate sampling in heterogeneous shelf waters. These have now been largely overcome, through the development of continuous sampling techniques, based on the use of pump methods (Pingree et al., 1975), of towed in situ instruments (e.g. Fasham et al., 1983a; Aiken and Bellan, 1986), and of remote sensing techniques (e.g. Holligan et al., 1983a). Another important feature of phytoplankton distributions concerns species succession. Numerous observations on temporal changes in species abundance and dominance confirm the classic pattern for temperate shelf waters of spring and autumn diatom peaks, and a mid-summer dinoflagellate maximum (Smayda, 1980). This pattern reflects changes in the availability of light and inorganic nutrients in the surface layers (Margalef, 1978), and can also be observed in a spatial context during the summer months as the transition from diatom populations in persistently well mixed waters to flagellate populations in seasonally stratified nutrient-depleted waters (Holligan, 1981). Superimposed on fluctuations in the abundance of the two main groups of larger phytoplankton is the development of coccolithophore blooms in early summer (Holligan et al., 1983b), which appear to occupy an

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Stations 3

I

JQb \

! 40c

i It

'i

0

-E

1

f

20

8 n 40

Fig. 4. Distribution of (a) temperature (T),(b) chlorophyll a (mg m-", and (c) nitrate (pM), across a section of the Ushant tidal front in the western English Channel, 2 August 1976. Station 30 (49' 40' N; 04"50' W) is in mixed water closest to land, and Station E5 (49"05' N; 06" 37' W) is in stratified water. From Holligan (1979).

intermediate successional position, and of low-biomass, climax communities dominated by autotrophic cyanobacteria and very small eukaryotic cells (Joint and Pipe, 1984) under conditions of strong surface stability. Patterns of succession are also recognizable at the species level (Maddock et al., 1981; Horwood et al., 1982; Wandschneider, 1983). Few studies of primary productivity in marine waters have included an analysis of phytoplankton species composition. As a result information on morphological (e.g. in relation to palatability for herbivores, sinking rates) and on physiological (biochemicalcomposition, nutrient requirements, capacity for extracellular release of carbon) characteristics is generally not available for evaluating productivity data within ecological or biogeochemical contexts. Furthermore, rather little is known about changes in photosynthe-

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tic properties that accompany shifts in species dominance or the collapse of a bloom. B. CONTROL OF PHYTOPLANKTON PRODUCTION

The effects of light, nutrients and temperature on phytoplankton growth have been extensively studied under laboratory conditions using uni-algal cultures. For natural populations of phytoplankton, light and nutrients rather than temperature are more important in controlling rates of production (Tett and Edwards, 1984), as they represent essential resources which are not always sufficient to support net growth in the water column. Situations of light limitation in the sea are readily identifiable in terms of vertical mixing of surface layers or of high turbidity due to particulate material other than phytoplankton. By contrast, nutrient limitation is more difficult to define, mainly because of the complex adaptive responses shown by phytoplankton populations to changes in the rate or form of nutrient supply. The main conceptual problems concern the distinction between rates of specific growth (biomass-independent) and rates of production (biomassdependent), and the dual effects of herbivory as a cause of mortality and as a source of regenerated nutrients (see King, 1986). Under natural conditions, nutrient limitation of population growth tends to be a transitory state, as cell losses from sinking and grazing, species replacement (succession), and nutrient regeneration lead to the establishment of a new species assemblage with different nutrient requirements that are met by the new conditions of nutrient supply. Marked changes in species composition and total algal biomass can occur over a period of a few days (e.g. Fasham et al., 1983a), reflecting the nutritional versatility of multi-species populations and the rapid rates of cell division and mortality. However, they are not necessarily accompanied by changes in growth rate; indeed, the available evidence suggests that low rates of nutrient supply are correlated with low standing stocks of phytoplankton (Eppley et al., 1979) rather than low growth rates (Goldman et al., 1979). For this reason, nutrient limitation of phytoplankton growth in the sea does not have a precise meaning, and the concept of nutrient control of standing stock or primary productivity is generally more appropriate. Much of the physiological information relevant to an understanding of phytoplankton growth is well described in the publications edited by Morris (1980), Falkowski (1980) and Platt (1981). Here it is sufficient just to emphasize those aspects that are of particular importance for the interpretation of primary productivity data and that have been the focus of more recent research. 1. Light The various problems in measuring photosynthetically active radiation

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(PAR) in aquatic environments are described by Kirk (1983) and Jewson et af. (1984). Values of the scalar irradiance (Eo)are the most useful in relation to rates of photosynthesis. In practical terms, these are most easily derived from vertical attenuation coefficients for scalar irradiance (KO)or for downward irradiance (&) the latter being measured with a cosine collector and giving a reasonable approximation of KO(Kirk, 1983). The scalar irradiance at any depth ( z )is then given by E,(z)

=

E,(0)e-KO'

where Eo(0) is the surface-penetrating photon flux density. Care has to be taken to avoid errors in estimates of Eo(z)for the upper part of the photic zone due to variations in KOor Kd that result from spectral changes in underwater irradiance (Jewson et af., 1984). For a given value of Eo(0)the total amount of PAR available for photosynthesis is approximately inversely proportional to KO(Kirk, 1983). Thus a typical range of 0.08-0.50 m- for KO in continental shelf waters implies a six-fold variation in light availability at any depth for a given value of Eo. Properties that contribute to KO include absorption by water, yellow substances and particulate matter as well as by phytoplankton cells. In general, it is possible to calculate the proportion of light absorbed by phytoplankton from a knowledge of KO,K, (the spectral absorption coefficient for chlorophyll) and chlorophyll concentrations (Morel, 1978) and, therefore, to estimate photosynthetic efficiency and quantum yields for natural populations (Dubinsky et af., 1984; Kishino et af., 1986). However, under conditions of strong scattering by particulate material, KOcannot be assumed to represent the sum of partial attenuation coefficients for absorbing components (Kirk, 1983). In considering the implications of regional variations of the light environment on primary production, it is important to have some method of determining the distribution of KO or Kd with adequate spatial and temporal resolution. There is no easy way of doing this. Light profiles and Secchi disc measurements, the latter being empirically converted to & (Walker, 1980; Preisendorfer, 1986), can only be made during the middle part of the day when the ship is stopped. Transmissometer measurements of beam attenuation coefficients offer the advantage of continuity in horizontal and vertical profiles. However, beam attenuation is the sum of absorbance and scatterance, which are interdependent optical properties of sea water, so that there is no simple relationship between the beam attenuation coefficient and vertical attenuation coefficients for (scalar) irradiance (e.g. Topliss et af., 198& 81). The best hope is offered by remote sensing of ocean colour, but algorithms for deriving the vertical attenuation coefficient (Austin and Petzold, 1981) have yet to be widely tested for NW European waters (Viollier and Sturm, 1984). The utilization of light by phytoplankton in the sea is most simply de-

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scribed (Fig. 5) by two relationships, the classical photosynthesis (Pkirradiance ( I ) curve, and the depth profiles for gross photoSynthesis (P,) and dark respiration (R)which define the compensation (Pg = R) and critical (sipg= SiR) depths. For comparative purposes, photosynthesis and respiration are expressed as biomass-specific rates and RB,with the biomass in units of carbon or chlorophyll. The difference between these rates is the specific net photosynthetic rate P:. When the depth of mixing (Z,) is less than the critical depth (i.e. P: is positive for the surface layer over a complete lightaark cycle or 24-h period), the phytoplankton biomass will increase if there are no losses due to sinking and grazing. Clearly the form of the P-I curve, as defined by the parameters a, P,,, and B (Fig. 5), determines the rate of primary production for any given set of environmental conditions (Eo,KO, Zm). Various methods are used for fitting P-I curves to sets of observational data on carbon assimilation, based on empirical relationships (Platt et al., 1980: Harrison et al., 1985) and on physiological models of light-dependent photosynthetic reactions (Fasham and Platt, 1983; Dubinsky et al., 1984). However, to estimate net production, carbon losses due to dark respiration must be taken into account (Dring and Jewson, 1982). Usually some constant value for R is assumed, but recent evidence suggests that the respiration rate is unlikely to be constant (Raven and Beardall, 1981; Falkowski et al., 1985) either from day to night, or with changes in physiological condition or species composition of the phytoplankton population. Other uncertainties in estimating P: concern the time-scales and quantitative importance of photoadaptation (Marra, 1978; Savidge, 1980; Falkowski, 1983, 1984; Marra et al., 1985; Kana et al., 1985), as well as variability in carbon losses due to photorespiration (Burris, 1980) and related processes leading to the exudation of organic carbon (Fogg, 1983). Despite these complex physiological problems, an analysis of adaptive strategies to different conditions of irradiance does show well-defined and ecologically significant differences between the main algal classes (Richardson et al., 1983). These are best illustrated as different forms of P-I curves (Fig. 6 ) that can be interpreted as responses due to changes in the number and size of the photosynthetic units. Although such interpretations may often be oversimplifications, they do represent a physiological basis for explaining taxonomic traits; for example, diatoms tend to grow well at high photon flux densities compared to other phytoplankton groups, whereas dinoflagellate populations show relatively efficient growth at low irradiances and often exhibit pronounced photoinhibitory responses. 2. Nutrients In temperate and polar seas the highest surface concentrations of the major inorganic nutrients (combined forms of nitrogen, phosphorus and silicon) required for phytoplankton growth are observed in the late winter when assi-

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Fig. 5. Idealized plots to show the relationship for a phytoplankton population between (a) photosynthesis (P) and irradiance (I);and (b) photosynthesis and phytoplankton respiration (R) in a mixed water column under conditions of midday sunlight. Net primary productivity becomes positive when the depth of mixing (thermocline) is less than the critical depth. See text for further details.

milation rates are minimal. The main sources of these nutrients are vertical mixing with nutrient-rich deep water and continuing regeneration from particulate and dissolved organic material. On the continental shelves lateral exchange with oceanic waters across the shelf break and river inputs are also important, the former being generally dominant except close to estuaries or in shallow, enclosed waters (e.g. James and Head, 1972). For oligotrophic ocean waters, rainfall can also be a significant source of nitrogen (Paerl, 1985). With the increase of solar radiation and development of the seasonal pynocline in the spring, there is rapid utilization of these nutrients by diatoms. The particulate organic material formed in the surface waters typically

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I

I/ I

/ PSU no.

/n PSU size

Fig. 6 . Idealized P-1 curves to illustrate (a) genotypic differences between phytoplankton groups, and (b,c) phenotypic responses for high (H) and low (L) irradiances involving changes in the size and number of photosynthetic units (PSU). For further details, see Richardson ei a/. (1983).

has a chemical composition conforming to the Redfield ratios (Redfield, 1958F-C : N : P in the proportions 106 : 16 : 1 by atoms. Although other types of phytoplankton may replace the diatoms if silica becomes depleted, the main declines in phytoplankton biomass and production occur when nitrate and phosphate reach minimal levels. Thereafter, nutrient control on primary productivity is generally thought to be due to low available nitrogen rather than phosphorus (Ryther and Dunstan, 1971), probably because rates of regeneration are somewhat slower for nitrogen, with the result that the ratio of dissolved nitrate to phosphate decreases during the summer (Pingree et al., 1977b). The relationship between nutrients and production in the sea is therefore generally considered in terms of nitrogen availability, although over short (days) and very long (geological) time-scales phosphorus may be more important. As inorganic nutrients are incorporated into organic material, regenerative processes lead to the release into the water of various reduced and organic forms of nitrogen and phosphorus. For nitrogen, these include substances that are readily reassimilated by phytoplankton (ammonium, urea, amino acids) as well as relatively refractory organic compounds. The latter form a substantial proportion of the dissolved organic nitrogen pool, reaching maximum concentrations in mid-summer (Butler et al., 1979), but are probably relatively unimportant for phytoplankton growth except in the most oligotrophic (stable) waters, where rates of primary production are low (Jackson and Williams, 1985). Ammonium and urea are important products of excre-

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tion and ammonification, and probably make up the bulk of the utilizable regenerated nitrogen (Corner and Davies, 1971). Ambient concentrations of nitrate and ammonium in nutrient-depleted, stratified waters are generally close to or below the limits of detection ( 0.1 PM) by standard colorimetric methods. In order to assess the uptake rates of new and regenerated nitrogen, two different approaches have been developed. The first concerns the careful measurement and evaluation of gradients in concentration with respect to rates of physical mixing. This is particularly applicable to estimates of the upward flux of nitrate across the seasonal pycnocline (King and Devol, 1979; Holligan et al., 1984b; King, 1986; Lewis et ul., 1986), but can also be considered in relation to lateral mixing across fronts (Loder er ul. 1982) and along isopycnal surfaces. A new chemiluminescent method for the detection of nitrate in sea water allows a precision of f2 nM and a much improved characterization of nitrate gradients (Garside, 1985), so that the main difficulty is in deriving reliable values for diffusion coefficients. The second approach depends upon the use of I5N as a tracer (Collos and Slawyk, 1980; Dugdale and Wilkerson, 1986) to assess rates of substrate assimilation by natural phytoplankton populations. There are experimental difficulties (Goldman, 1980) concerned with long incubation periods and the addition of relatively high concentrations of carrier substances which are not representative of natural conditions, but these have been largely overcome for eutrophic waters (Dugdale and Wilkerson, 1986). Studies at sea have provided consistent, albeit largely indirect, evidence that the nitrogen requirements of phytoplankton are mainly met by a combination of new nitrate (mixing from deep water) and regenerative ammonium (in siru release by heterotrophs) sources (Eppley et al., 1979; Eppley and Peterson, 1979; Harrison et al., 1983, 1987). Urea also appears to be important in inshore waters (McCarthy, 1972; Turley, 1985, 1986), but for offshore waters the contribution of both urea and amino acids (Fuhrman and Ferguson, 1986; Flynn and Butler, 1986) remains uncertain. The dependence of growth on maintained new inputs of nitrate to balance nitrogen losses from the euphotic zone due to sinking faecal pellets and other particulate matter and to the downward mixing of dissolved organic nitrogen was clearly shown by Eppley and Peterson (1979). Much attention is now being given to evaluating the relationship between ambient nitrate concentrations and the “f-ratio” or ratio of new (nitrate-based) production to total production (Harrison et al., 1987). A much clearer picture has now also emerged from laboratory studies with algal cultures of the relationship between nutrient assimilation and growth in physiological terms. Early growth models based on the classical Monod equation, which related the specific growth rate ( p ) to the external concentration of the limiting nutrient, have now been largely replaced by ones which show growth rates to be dependent on internal nutrient levels (Droop, 1983). The best-known form is the cell quota model: N

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where pm is the maximum growth rate, Q the phytoplankton nutrient content, and Kq the subsistence quota (or minimum nutrient content to maintain viability). The rate of nutrient uptake (u) is considered separately, generally as the hyperbolic Michaelis-Menten relationship:

where u, is the maximum uptake rate, S the external nutrient content and K , the half-saturation constant for nutrient uptake. These equations represent the simplest interpretations of experimental data (mainly from chemostat cultures) but, despite their recognized limitations (Laws and Bannister, 1980; Droop, 1983), they are of ecological significance for several reasons. Only one nutrient is considered limiting at any one time; for nitrogen sources the low ambient concentrations in sea water are compatible with low K , values (e.g. Goldman, 1977); also they imply that growth rates are not necessarily dependent upon external concentrations (Dortch et al., 1485; Collos, 1986). Another important principal to emerge from chemostat studies of steadystate growth concerns the relationships between nutrient supply, standing stock, and dilution (loss) rates. At steady state, the phytoplankton biomass represents the ratio between the nutrient supply rate and the specific growth rate, the latter being set by and therefore equal to the dilution rate. In the sea, grazing mortality is analogous to the dilution rate and acts as a feedback control (excretion) on nutrient supply. Thus, under stable environmental conditions, differences in the rate of nutrient supply to the surface layers will be reflected by comparable differences in phytoplankton standing stock, provided that the growth/grazing rates do not vary greatly (Eppley, 1981). Furthermore, for any given growth rate, standing stock will be linearly proportional to net productivity. Thus observed variations in standing stock are indicative of changes in both nutrient supply and productivity (see King, 1986). There are two outstanding problems concerning the nutrient physiology of natural phytoplankton populations. The first is the interaction of nutrient uptake and growth under conditions of fluctuating nutrient supply (due, for example, to variable mixing across the thermocline, or the vertical migration of zooplankton), which is likely to lead to the condition p # pQ over one or more cell cycles. Such transient nutritional states are discussed by Dugdale (1977) and Droop (1983). The second is the form of nutrient-light interactions, and is particularly pertinent to growth in stratified waters where the main sources for nutrients and light are at the bottom and top of the euphotic

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zone respectively. The opposing vertical gradients in these two properties lead to the potential for interactive effects on phytoplankton growth at all depths over the natural 24-h light-dark cycle. Some recent models treat light and nutrients in a non-synergistic manner (Tett, 1981; Tett et al., 1986), but the physiological complexities are well illustrated by attempts to interpret cell properties (e.g. variance from Redfield ratios for chemical composition) in terms of the combined effects of nutrients and light (Laws and Bannister, 1980; Tett et al., 1985). 3. Temperature From studies with algal cultures, temperature is known to have profound effects on cellular metabolic rates (Li, 1980), and equations for temperature effects based on the Arrhenius formulation for chemical reactions are included in growth models (e.g. Goldman, 1979). Furthermore, different species, as well as different clones of the same species, show marked differences in temperature optima and tolerances for growth. For this reason, conclusions about temperature effects based on laboratory observations must be interpreted with care in an ecological context-for example, an isolate from temperate waters of the coccolithophore Emiliania huxleyi showed little or no growth below 7°C (Paasche, 1968), whereas natural populations of this species are known to occur at temperatures < 0°C (Heimdal, 1983). Fluctuations in sea temperature are less extreme and more gradual than those of air temperature affecting terrestrial environments. At mid-latitudes the annual range of sea surface temperature is typically about IOOC, increasing to about 20°C close to continental land masses. This is sufficient to account for much of the variability in maximum photosynthetic rates both seasonally (Eppley, 1972; Harrison and Platt, 1980) and in relation to latitudinal temperature gradients (Li, 1985). On the other hand, rates of temperature change rarely exceed 1°C per day, so that variations in photosynthetic rates over shorter time-scales are generally considered to be due to other environmental conditions such as light and nutrients. In a spatial context, however, temperature gradients can be relatively steep, with differences in the order of 5510°C horizontally over a few kilometres across surface frontal boundaries, and vertically over a few metres across the seasonal pycnocline in continental shelf waters. In general the species composition of the phytoplankton changes across such temperature gradients, and only in the case of dinoflagellate populations exhibiting die1 vertical migrations across the thermocline (Blasco, 1978) are cells of a particular population exposed regularly to temperature changes of potential physiological significance. A laboratory study by Heaney and Eppley (198 1) showed that swimming speeds of dinoflagellates were markedly reduced at lower temperatures. 4 . Grazing Although sinking and natural death (Walsh, 1983; Billet et al., 1983) are

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locally important causes of phytoplankton mortality, leading to consumption by detritivores beneath the euphotic zone or to direct incorporation of plant material into bottom sediments, the main losses of plant cells are due to predation by planktonic herbivores in the surface layers. In considering rates of primary production, grazing not only removes part of the standing stock of phytoplankton but also indirectly promotes the continued growth of the remaining population through the release of nutritionally valuable excretory products (Corner and Davies, 1971). The relationship between primary production and grazing is therefore complex (Frost, 1980). Changes in phytoplankton biomass ( B ) with time ( t ) as a function of the rates of phytoplankton growth ( p ) and predation by grazing ( g ) can be expressed as

The various factors that determine the value of the coefficient g , including the size, type and abundance of both the phytoplankton and herbivores, are discussed by Frost (1980). Numerical modelling is an important technique for examining the range of possible dynamic states between prey and predator under natural conditions (e.g. Steele and Frost, 1977). In simple terms, grazing can be considered as the product of herbivore biomass, herbivore filtration (volume clearance) rate and phytoplankton concentration (King, 1986). However, the filtration rate is itself a function of phytoplankton concentration, and differences in the form of this relationship represent the range of feeding strategies for different herbivore species (Frost, 1980). Under stable environmental conditions, as represented by stratified, nutrient-depleted surface waters, this results in the convergence of p and g, so that the biomass of phytoplankton tends to a constant value. In other words, assuming that grazing is the major cause of phytoplankton mortality, the increase in phytoplankton biomass due to growth is balanced by losses due to grazing. By analogy with chemostat cultures at steady state (Dugdale, 1977), for which the dilution rate is equivalent to the herbivore filtration rate, this leads to the concept that grazing indirectly determines the phytoplankton growth rate (Jackson, 1980). Away from the tropical ocean gyres, seasonal changes in climatic and physical oceanographic conditions cause variations in the degree of surface mixing. These lead in turn to fluctuations in phytoplankton growth rates and to an uncoupling of growth and grazing as p and g differ. For example, in temperate regions in the spring or in recently upwelled waters, the diatom outburst is attributable to a greater increase of ,u than of g in response to stratification and favourable light conditions (Colebrook, 1986b). Subsequently, the phytoplankton biomass is reduced when nutrient depletion leads to a decrease in p while losses due to g and perhaps sinking (e.g. Billett et al., 1983) remain relatively high. However, in regions such as the subarctic North Pacific, the spring increase in phytoplankton is small and surface nutrient concen-

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trations remain high throughout the summer. This situation is thought to be due to rapid adaptations in the feeding strategy of overwintering herbivores which, as p increases, maintain comparable values of g (Frost, 1984). Changes in rates of primary production will tend to be slight, reflecting variations in p for a relatively constant plant biomass that is determined by grazing rather than climatic (light) or hydrographic (nutrients) variability. In view of the importance of grazing as a cause of phytoplankton mortality and as a means of nutrient regeneration, methods for quantifying rates of grazing under natural conditions (Roman et al., 1986) are necessary for a more complete understanding of the production dynamics of marine plankton communities. Attempts to assess directly grazing or filtration rates by mixed herbivore populations are restricted by a lack of comparative information on the feeding strategies of individual species, and by uncertainties in applying results from laboratory feeding studies to natural situations. Additional complications are the patchiness of herbivore distributions in the sea and changes in feeding behaviour (including die1 vertical migrations by the larger herbivores) in response to food availability. A new method of assessing grazing mortality based on changes in the distributions of phytoplankton pigments and degradation products in the water column (Welschmeyer and Lorenzen, 1985), has been devised to give integral measurements over periods of days to weeks. If this technique proves to be generally applicable, it could provide the first directly comparable information on grazing rates within different plankton communities. An alternative approach has been to measure nitrogen excretion by natural zooplankton populations (e.g. Dagg et al., 1980; Vidal and Whitledge, 1982). Despite unavoidable limitations of methodology and considerable variance in the results, good agreement is found between the nitrogen requirement of phytoplankton and nitrogen inputs due to the excretion of ammonium and urea and to the mixing of nitrate across the pycnocline (e.g. Harrison et al., 1985). However, no critical analysis has yet been made to show that such results are consistent with accepted values for the efficiency of nitrogen recycling by herbivores (see Corner and Davies, 1971) or with the turnover of dissolved organic nitrogen compounds (see Jackson and Williams, 1985). In other words the precise role and importance of herbivores in the various processes that lead to the regeneration of combined inorganic nitrogen within the euphotic zone, including excretion, ammonification and nitrification (Ward, 1985), remains uncertain. Recently, much attention has been given to the role of microheterotrophs (protozoa, microflagellates, bacteria) as consumers of plant carbon (for a general discussion, see Williams, 1984). Although these organisms are certainly abundant (Azam et al., 1983), much less is known about their feeding and growth than for herbivorous zooplankton which includes copepods, gastropods, and various gelatinous organisms. For temperate continental shelf waters, the available evidence still sup-

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ports the well-established concept (Steele, 1974) that the bulk of energy transfer occurs through herbivorous zooplankton (mainly copepods) feeding on phytoplankton larger than 5 pm in diameter (Ducklow et al., 1986). Under certain conditions, such as low chlorophyll water overlying a stable seasonal thermocline (Joint and Pomroy, 1983) or within blooms of the colonial flagellate Phaeocystis (Joiris et al., 1982), the utilization of plant carbon may largely be in the form of microheterotrophs feeding on autotrophic picoplankton or assimilating photosynthetic exudation products. However, in these cases, the efficiency with which plant energy is transferred to higher trophic levels is probably relatively low (i.e. much of the organic carbon will be converted to respiratory COz), the main effect of microheterotroph activity being to enhance rates of nitrogen and phosphorus remineralization (Ducklow et al., 1986).

111. METHODS FOR ESTIMATING PRIMARY PRODUCTIVITY A. NUTRIENT BUDGETS

The constant proportions of the elements carbon, nitrogen and phosphorus in growing phytoplankton cells (Redfield, 1958) allow organic production to be considered in terms of the incorporation of nitrogen or phosphorus into plant material as well as that of carbon. This approach is particularly pertinent to studies of marine productivity, as these two nutrients are thought to control phytoplankton growth in most situations (Eppley and Peterson, 1979), and deviations from the “Redfield ratios” of 106C : 16N : 1P by atoms can be indicative of nutrient-limited growth (Goldman et al., 1979; Tett et al., 1985). The development of reliable techniques for measuring dissolved inorganic and particulate inorganic forms of nitrogen and phosphorus in sea water opened the way for assessing primary productivity in terms of nutrient fluxes (Cooper, 1933). They apply specifically to rates of net production, since there are no major respiratory losses for nitrogen and phosphorus as there are for carbon. The first production estimates were based on the disappearance of nutrients during the spring bloom (see Harvey, 1950). Subsequent studies took into account vertical fluxes across the seasonal thermocline and were extended to cover the whole annual production cycle (Steele, 1956). Apart from the inherent difficulties in quantifying the effects of horizontal diffusion and advection, which are likely to be of particular importance in frontal regions, the main weaknesses of the nutrient budget approach are as follows: 1. Nutrient recycling within the euphotic zone is not taken into account, and either has to be assessed from appropriate experimental measurements or given some assumed value.

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2. It is dependent on accurate estimates (usually indirect) of vertical diffusivity. 3. For situations where the pycnocline is well within the euphotic zone (e.g. above the 1 % light level), care must be taken to specify accurately the vertical nutrient gradients which are modified by phytoplankton assimilation within the pycnocline. The first of these problems has been extensively investigated, particularly in relation to nitrogen, and statistical analyses of observational data on the relative contribution of renewal (physical mixing) and regeneration processes in supplying nutrients for phytoplankton growth have shown a significant relationship between total production and the proportion of production due to renewal or regeneration (Eppley and Peterson, 1979; Platt and Harrison, 1985). The second two are strongly site-specific, and can only be resolved through precise measurements of relevant properties within the water column (King and Devol, 1979; Eppley et d., 1979; Holligan et d.,1984b; Garside, 1985; King, 1986). With recent improvements in analytical and experimental techniques for using 15N (Dugdale and Wilkerson, 1986) and new understanding of how total production varies with the proportions of nitrogen available from renewal and regenerative processes (Harrison et al., 1987), it appears that measurements of ISNO; assimilation can be used to assess primary production. Although these methods are not yet widely in routine use, and there is still controversy about how to interpret f-ratio values (the ratio of nitrate to total nitrogen assimilation), this approach represents an important development for primary production studies, as it allows direct comparison of nitrogen and carbon assimilation rates. B. OXYGEN A N D CARBON FLUXES

Changes in dissolved oxygen provided the first direct measurements of photosynthetic production in the sea (e.g. Marshall and Orr, 1930; Cooper, 1933; Riley, 1946), and were supported by studies with cultures (Marshall and Orr, 1928; Jenkin, 1937). However, the low sensitivity of the standard Winkler technique meant that changes in oxygen could only be reliably estimated for relatively dense phytoplankton populations. Recent modifications allow measurements of dissolved oxygen in sea water with a coefficient of variation < 0.1 % on a routine basis (Bryan et al., 1976), so that even in oligotrophic ocean waters light and dark changes in oxygen levels can now be accurately determined (Williams et al., 1983). Conversion of oxygen values to carbon values depends on the photosynthetic quotient, which varies with the biochemical state of the cells, in particular with respect to the nitrogen source for growth (Williams et al., 1979; Williams, 1984). Tracer techniques based on I4CO2 largely superseded oxygen methods

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during the 1950s, as they gave greater sensitivity for production measurements (Steeman Nielsen, 1952). They have been reviewed recently by Gieskes et al. (1979) and Peterson (1980), and the various problems of interpreting data on I4CO2assimilation for marine waters are further discussed by Davies and Williams (1984) and Hitchcock (1986). As this is still the standard method for estimating rates of photosynthesis in the oceans, its main limitations must be recognized: 1. Physiological and ecological artefacts due to the enclosure of water samples in bottles cannot be fully avoided and are difficult to evaluate quantitatively. These range from direct effects on rates of carbon assimilation, to the problems of simulating fluctuations in irradiance due to mixing within the water column (Joiris and Bertels, 1985), and difficulties of interpretation introduced by secondary consumption of particulate and dissolved plant carbon during the incubation period. 2. Observed rates of carbon assimilation are likely to represent intermediate values between net and gross production, with the bias to one extreme or the other being dependent on incubation time, irradiance and rates of carbon turnover within intracellular pools (Dring and Jewson, 1982). There is still no reliable way of determining rates of phytoplankton respiration in the presence of heterotrophic organisms. 3. Compensation irradiances for different species, or for the same species under different conditions of growth (e.g. different nitrogen sources), vary by at least an order of magnitude (Hobson and Guest, 1983; Richardson ez al., 1983), so that any correction for dark respiration by natural populations can only be an approximation. 4. Uncertainties of rates of carbon exudation (Fogg, 1983) persist, owing to a combination of methodological problems and the difficulty of accounting for reassimilation by heterotrophic organisms during the experimental incubation period (Davies and Williams, 1984).

Several comparative studies of oxygen production and I4CO2assimilation have been undertaken in order to resolve some of these problems (e.g. Sakamot0 et al., 1984; Kuparinen, 1985; Shim and Kahng, 1986). For both continental shelf (Davies and Williams, 1984) and oceanic (Williams et al., 1983) waters, good agreement has been found between the two methods. Together with compatability between in situ and in vitro rates of oxygen production, this suggests that the 14C technique is not subject to any inherent source of error, although simultaneous heterotrophic activity may still introduce ambiguities into the interpretation of experimental data (Smith et al., 1984). Deviations from expected molar ratios for oxygen production to particulate carbon assimilation (the photosynthetic quotient) can be caused by differences in cell storage compounds, nitrogen sources for growth, and rates of organic carbon exudation. Such effects represent a further restriction on the use of dark oxygen changes to correct compatible measurements of photo-

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synthetic carbon fixation for phytoplankton respiration, even in the absence of heterotrophic organisms. One important and consistent observation from parallel oxygen and carbon measurements (e.g. Raine, 1983; Holligan et al., 1984b; Megard et al., 1985) is that photosynthetic quotients tend to increase at low irradiances (i.e. with depth in the water column). This result may be partly due to nitrate being a more important source of nitrogen as opposed to ammonium or other reduced compounds at the level of the pycnocline, but also probably reflects the selective utilization of photoreductant for nitrogen rather than carbon assimilation at low light levels (Megard et al., 1985). The latter effect is one explanation for anomalously high dissolved oxygen values in subsurface waters (Shulenberger and Reid, 198I ; Platt and Harrison, 1985, 1986; Craig and Hayward, 1987), and would lead to relatively low carbon to nitrogen ratios for the phytoplankton. The results from any set of oxygen production or carbon assimilation measurements must be integrated over both depth and time to give rates of production in appropriate units such as g C m-' day-'. Certain simplifications have to be made, mainly concerning the photosynthesis-light relationship, but in general it appears that these are unlikely to introduce significant errors (Mommaerts, 1982) compared to those that can affect experimental incubation procedures. Biological production may also be estimated by following in situ changes in the dissolved concentrations of oxygen and carbon dioxide in surface waters. Carbon dioxide can be determined directly as total inorganic carbon, or indirectly through appropriate measurements of pH and alkalinity (e.g. Brewer and Goldman, 1976). This way of assessing production has the advantage that many measurements can be made, so allowing better spatial coverage than with bottle incubations. Ambient carbon dioxide levels are also affected by the activity of heterotrophic organisms, and by exchanges across the air-sea interface and the pycnocline. Despite these restrictions, good agreement has been reported both between simultaneous dissolved oxygen and carbon dioxide changes (Johnson et al., 1979) and between carbon dioxide changes and I4CO2assimilation (Weichart, 1980; Codispoti et al., 1982), over periods of days to weeks. The need for improved data on spatial variability in rates of primary production, particularly in relation to physical environmental conditions, will probably lead to greater use of this approach in the future. C. BIOMASS DISTRIBUTIONS

Measurements of rates of net carbon assimilation represent a change in biomass per unit time ( A B t - I ) . Although often scaled against some measure of total biomass such as chlorophyll ,for comparative purposes, they do not incorporate or depend upon any absolute measure of biomass in equivalent

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units. Under circumstances of minimal grazing and sinking losses, as are occasionally observed in the growth phase of early spring diatom blooms (Tett et al., 1975) and of summer dinoflagellate blooms (Holligan et al., 1983a), changes in phytoplankton biomass will approximate to net primary productivity (Cushing and Vucetic, 1963; Cushing, 1983). More usually, however, such losses tend to match production (i.e. a quasi-steady-state condition is established between phytoplankton growth and mortality), and the question arises as to whether there is any relationship between the biomass or standing crop of the phytoplankton and primary productivity. This is best considered in terms of the standard equation for the specific growth rate (p)at steady state (Eppley, 1980): 1 AB p=--*B At

which can be written to a good approximation in the integrated form: 1 (B+AB) p =-In B t and gives on rearrangement: AB = B(e" - 1) Here AB is related to two variables, the biomass and the specific growth rate (Li and Goldman, 1986) of the phytoplankton population. Reliable estimates of growth rates in the sea are hard to obtain, mainly because phytoplankton carbon cannot be measured directly. A review of published data (Goldman et al., 1979) indicates that, providing that light availability is not the primary controlling factor, the annual rate of values for p is likely to be considerably less than an order of magnitude (typically 0.1 < p u > 1.0 day-') for a given region. By contrast, values of B can vary by up to two orders of magnitude or even more during the annual production cycle. On this basis some correlation between AB and B is to be expected. A relationship between these two parameters has been demonstrated for different oceanic areas, using chlorophyll as a measure of biomass (Ryther and Yentsch, 1957; Lorenzen, 1970; Eppley et al., 1985). However, there are regional differences in proportionality factors which Eppley et al. (1985) suggest are due to environmental conditions, including insolation. The main exceptions to any positive correlation between phytoplankton standing stock or biomass and the rate of primary production are likely to be when growth is limited by light, either through self shading or through deep mixing of the surface layer, and during the declining phase of blooms. With the development of techniques such as in vivo fluorometry (Lorenzen, 1965) and remote sensing of ocean colour (Gordon et al., 1983) for estimating chlorophyll over a wide range of spatial (horizontal and vertical) and temporal scales, the use of biomass as an indicator of rates of production

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could provide much new information about primary productivity in the oceans. Although the estimates may only be semi-quantitative due to difficulties of calibration, they are a source of background data on the variability of production processes in the sea which will enable more objective sampling and experimental work from ships. Furthermore, there is the possibility that ocean colour data can be directly related to productivity (Platt and Denman, 1983; Smith et al., 1983a; Platt, 1986). One major uncertainty with remote sensing techniques is variability in carbon/chlorophyll ratios for phytoplankton (Banse, 1977), which are difficult to measure since living phytoplankton generally constitutes only a minor proportion of the total particulate organic carbon in surface waters. Indirect estimates, using a variety of techniques, are generally in the range 20-100, with a mean of about 40 and values for diatoms generally lower than for dinoflagellates. D. PRIMARY PRODUCTIVITY MODELS

Recently, much effort has been put into the development of numerical models of phytoplankton growth in the sea in an attempt to simulate observed spatial and temporal changes in distributions, and to identify the parameters that control variability in biomass and/or production. These models have various aims which, in turn, reflect differences in their degree of complexity, in methods of defining the physical and chemical environmental properties, in the formulation of the growth process and in their mathematical solutions (Wroblewski, 1983). In relation to studies on primary productivity, the main emphasis has been to simulate observations at sea, and in this sense the results can only be as good as the original observations. However, attempts to match the results of real measurements and numerical models help to clarify concepts about the factors controlling phytoplankton growth in shelf seas over both short (Fasham et al., 1983a; Radach, 1983) and long (Horwood, 1982) time-scales. Of particular interest are those models that compare phytoplankton growth under contrasting physical and chemical conditions (e.g. Tett, 1981; Agoumi et al., 1985; Tett et al., 1986); they provide an objective evaluation of the effects of different environmental factors on primary productivity and indicate relative differences in total production.

IV. ENVIRONMENTAL CONDITIONS FOR PHYTOPLANKTON GROWTH IN THE NW EUROPEAN SHELF SEAS A. MIXING PROCESSES, SEASONAL STRATIFICATION

Physical properties of shelf seas relevant to biological processes, and in particular phytoplankton growth, are described by Pingree (1987b, 1980), Lee

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(1980), Simpson (1981) and Loder and Platt (1985). Here it is sufficient tc give a brief account of changes during the annual cycle that have a fundamental influence, directly or indirectly, on phytoplankton abundance. For convenience this is done with particular reference to temperature, which is the main factor determining vertical and horizontal density gradients, although salinity variations can be important, especially in the N E North Sea and Norwegian coastal waters. Thus the term thermocline (vertical temperature gradient) is used in place of pycnocline (vertical density gradient), which includes the influence of salinity on the vertical stability of the water column. Each winter the combined effects of surface cooling (heat loss to the atmosphere), surface wind mixing and bottom tidal mixing cause the water column on the shelf to become vertically homogeneous with respect to density. Any vertical gradients in temperature and salinity tend to be slight and shortlived. Horizontal gradients in these properties are also weak, although satellite images do show well-defined temperature boundaries around coasts which mark the outer extent of relatively cool, less saline, inshore water. From late winter onwards vertical stratification of the water column can develop, due mainly to river outflows of fresh water and solar warming of surface layers. Initially this change probably occurs mainly during neap tide periods. However, by April, thermohaline stratification becomes a persistent feature in regions of weak tidal mixing such as the central Celtic Sea and northern North Sea (Sager and Sammler, 1968). The horizontal extent of the seasonal thermocline is maximal by about the end of May (e.g. Pingree, 1975), but solar heating continues to strengthen the vertical density gradients until July or early August (e.g. Pingree et al., 1976), when surface-to-bottom temperature differences of 5-10°C are observed in large areas of the Celtic and North Seas. In regions of strong tidal mixing, the water column generally remains well mixed throughout the summer, although a combination of strong solar heating, low wind speeds and neap tides may allow temporary (hours to days) stratification almost anywhere. In summer, the boundaries between mixed and stratified waters tend to be characterized by horizontal temperature gradients (Pingree et af., 1975) as a result of differential heating; in stratified waters the heat input is effectively trapped in the upper 10-30 m of the water column above the thermocline, so causing relatively rapid warming (up to 2°C month-') of the surface windmixed layer and slow warming (as low as 0.1"C month-') of the bottom tidally mixed layer. By contrast, where tidal mixing prevents the formation of a thermocline, the heat input is spread through the whole water column, which may be up to 100 m deep. The rate of increase in temperature is therefore intermediate between those for surface and bottom waters in neighbouring stratified areas, so that horizontal gradients in both surface and bottom temperatures are established. These gradients become most pronounced at the surface in deep waters (see Fig. 4) and at the bottom in shallow waters, and are generally known as tidal fronts (Simpson and Hunter, 1974).

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Numerical models that predict patterns of summer stratification from information on water depth ( h ) and tidal streams (u, the mean M2 tidal current velocity) have now been well tested by comparison with observations from ships and satellite (Pingree and Griffiths, 1978). The average positions of tidal fronts (Fig. 7) are consistent with a particular value of the stratification parameter, S, which is defined as S = log,,, (h/CdU3)(Cd is a dimensionless drag coefficient), and generally show only small deviations in position in response to wind effects or spring-neap tidal cycles (Simpson and Bowers, 1979). However, as with all types of frontal boundary, they are subject to various forms of instability (Pingree, 1978a) which, together with any advective effects, can lead to gross movements over scales of tens of kilometres (e.g. Pingree et a/., 1977a). Such effects are important in determining rates of cross-frontal exchange of water properties, including inorganic nutrients and planktonic organisms. In a similar manner, the seasonal thermocline, which represents the subsurface extension of surface fronts (see Fig. 4), is affected by physical mixing processes that determine vertical exchange or diffusion within the water column (Pingree and Pennycuick. 1975). The dissipation of internal wave energy (Pingree and Mardell, 1985) is now thought to make an important contribution to this process, as well as the effects of winds and tides. By autumn surface cooling and increased wind mixing lead to the erosion of tidal fronts and the seasonal thermocline. There is a general weakening of the density (thermal) gradients and some gross displacement of the boundaries; surface fronts retreat as the region of stratification becomes smaller (Pingree, 1975), and the thermocline deepens in response to increased mixing at the surface (Pingree et a/., 1976). However, the timing and progress of such events are irregular, so that the effects on biological properties may be quite different from one year to the next. Against this background of seasonal change in the physical environment, it is necessary also to distinguish chemical and biological factors that affect phytoplankton distributions in order to gain some overall understanding of primary production processes in the shelf seas of NW Europe. From a general analysis of plankton patchiness, Mackas et al. (1985) concluded that physical effects are dominant only at small scales. Examples are Langmuir circulation patterns in which phytoplankton cells showing directional motility or buoyancy are accumulated (Le Fevre, 1986), and boundary zones such as the seasonal thermocline where rates of turbulent diffusion may be low enough to allow aggregations of cells to persist (Pingree, et al., 1975). By contrast, at larger scales, phytoplankton distributions are largely determined by a combination of the availability of resources (i.e. light and nutrients, which in turn are controlled by physical conditions), by the growth responses of individual species, and by the activities of herbivores (see Taylor et a/., 1986).

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Fig. 7. Distribution of mixed, frontal and stratified waters for the NW European shelf in summer, based on the numerical model of Pingree and Griffiths (1 978) for the stratificationparameter, S (see text). B. LIGHT AVAILABILITY

The seasonal and daily ranges of sea surface irradiance can be inferred from meteorological data. With the latitude and climatic conditions of the NW European shelf, daily irradiance values vary by about one order of magnitude between mean winter and summer conditions, and between overcast and clear days at any one time of the year (e.g. Mommaerts, 1973). On an annual basis, total irradiance decreases from south to north by approximately 30% between 50"Nand 60"N. Except for surface albedo losses, which are usually 10% (Payne, 1972), it

-

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Fig. 8. Atmospherically corrected Coastal Zone Color Scanner image (Channel 2, 510530 nm) for the southern North Sea on 5 March 1982 (courtesy of S. Groom). Light areas indicate reflective waters with a high suspended sediment load, and dark areas relatively clear waters which are least reflective (i.e. darkest) where there is significant absorption by plant pigments. CI, clouds.

is the properties of the water that determine the proportion of light available for photosynthesis. Over most of the continental shelf surface, salinities remain > 34K, so that variations in light absorption due to the water itself, including dissolved substances, are unlikely to be great (Hajerslev, 1983, 1982). Thus the main factor affecting the light environment for photosynthetic organisms, apart from self-shading which is a function of chlorophyll concentration, is scattering by suspended particulate matter (Topliss et al., 19808 1 ; Topliss, 1982; Hajerslev, 1982). The extremely heterogeneous distribution of surface turbidity is well shown by satellite ocean colour images (Fig. 8; Mitchelson et al., 1986), from which maps of the attentuation coefficient can be derived (Viollier and Sturm, 1984). Due to the difficulty of making appropriate continuous in situ measurements, there is relatively little published data on attenuation coefficients for the NW European shelf seas as a whole. Surveys have been made with the Secchi disc (e.g. Tijssen, 1968; Holligan et al., 1978), and with instruments that measure turbidity or beam transmission (Lee and Folkard, 1969;

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Pingree et al., 1986). Together with irradiance profiles for discrete stations which are often made in conjunction with primary production measurements, these suggest that KO is generally in the range 0.084.60 m-', with values >0.20 m-' confined to well-mixed, turbid coastal waters and to exceptional phytoplankton blooms (e.g. Holligan et al., 1983a). In the absence of significant light absorption by chlorophyll, higher KOvalues are consistently observed close to the shore, but gradients normal to the coastline are very variable (Pingree et al., 1986) and are often characterized by large variations at boundaries between different water masses (Brylinski er al., 1984). Within offshore coccolithophore populations, rather unusual light conditions prevail due to a combination of low absorption by relatively low chlorophyll concentrations and strong scattering (high reflectance) by coccoliths (Holligan et al., 1983b). The range in attenuation coefficients sets broad limits on light availability for photosynthesis, assuming that the depth of the surface mixed layer (i.e. the degree to which phytoplankton cells are held within the euphotic zone) is known. If other factors, such as nutrients and grazing, did not limit primary production, the combined effects of light attenuation and depth of mixing would effectively determine production rates. This premise has led to the use of the parameter kh (the light attenuation coefficient, k , scaled by the water depth, h) for defining the light environment of natural phytoplankton populations in shelf waters (Pingree et al., 1978b; Bowman et al., 1981). Together with information about surface irradiance, such an approach allows an objective comparison of light regimes and the ability to predict for any given region the start and end of the phytoplankton growth season (see Figs 8 and 21 in Pingree (1978b)). For stratified waters, h is effectively given as the mixed layer depth, so that the change in light availability resulting from the onset or breakdown of stratification can also be assessed. On the NW European shelf, phytoplankton growth can be restricted by light throughout the year, both in turbid estuaries such as the Bristol Channel, for which a 20-fold range in annual productivity values has been described (Joint and Pomroy, 1981), and in deep, relatively clear waters where strong tidal mixing prevents the formation of a seasonal thermocline (Pingree et al., 1978; Martin-JCzequel, 1983). By contrast, in some regions the water is sufficiently clear and shallow (i.e. low kh value) that some net production may occur even in the winter-see Postma (l978), who infers this to be the case for parts of the southern North Sea where winter levels of inorganic nutrients remain relatively low. In most deeper waters ( > 6 0 m), which became stratified in the summer, the development and breakdown of the seasonal thermocline is probably the main factor in determining the length of the growth season (e.g. Pingree et al., 1976), but in shallow waters the combination of seasonal changes in irradiance and low kh values is likely to be more critical. The seasonal thermocline and associated subsurface chlorophyll maxi-

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mum represents a special type of light environment. Due to light attentuation within the wind-mixed layer, the plant cells are exposed to a restricted range of irradiance and will, in general, show positive net photosynthesis only in relatively clear weather (Holligan et al., 1984b). This has important implications both for estimates of water column productivity and for understanding the potential effects of light on nutrient fluxes across the thermocline (Taylor et ul., 1986). With the recent advances in understanding how tides largely determine the development of the seasonal thermocline and the positions of frontal boundaries between stratified and mixed water masses, it appears that predictions of the effects of light on phytoplankton growth are limited mainly by a lack of information about variations in values for K O .A more detailed analysis of satellite imagery for the visible wave band (Hrajerslev, 1982; Viollier and Sturm, 1984) will be one approach to resolving the problem. C. NUTRIENT AVAILABILITY

As already indicated, nutrient availability acts as a secondary control on primary production in temperate shelf seas once there is sufficient light for the plant cells to grow. To a first approximation, total annual primary production is likely to be proportional to the quantity of new nutrients (i.e. derived from deep water and/or winter regeneration in surface layers) assimilated by the phytoplankton (Eppley and Peterson, 1979). On the NW European shelf, maximum surface concentrations of inorganic nutrients are usually observed in late winter before uptake by phytoplankton in the spring starts to exceed rates of regeneration from dissolved and particulate organic materials in the water column and sediments. Levels of nitrate nitrogen and phosphate phosphorus reach 6-12 ,UMand 0.4-0.9 ,UMrespectively (e.g. Johnston and Jones, 1965; Pingree et al., 1976; Postma, 1978; Foster, 1984; Brockmann and Wegner, 1985), but are higher in estuarine and some inshore waters. In terms of the annual turnover of dissolved nitrogen and phosphorus, net losses from shelf waters in the form of fluxes of particulate matter to the sediments and of dissolved organic matter to deep ocean water are mainly balanced by oceanic inputs, with Atlantic water probably accounting for about 80% of the total nutrient supply for the shelf ecosystem (e.g. Gerlach, 1981). Most of the remainder comes from fresh-water inputs (precipitation, land drainage), but only locally within semi-enclosed regions distant from the shelf break, such as the southern North Sea, are these the dominant nutrient sources (Postma, 1978, 1985). In the spring and summer the inorganic nutrients are assimilated by the phytoplankton, with surface concentrations being reduced typically to < 0.5 PM nitrate nitrogen and CO.1 ,UM phosphate phosphorus. In mid-summer, appreciably higher values are restricted to mixed coastal and estuarine waters

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characterized by high kh values. The nitrate to phosphate ratio tends to decrease with depletion (e.g. Pingree et al., 1977b), suggesting that nitrate is in shorter supply, possibly as a result of less rapid regeneration. Exceptions to this are in parts of the southern North Sea, where low phosphate appears to limit phytoplankton growth (Postma, 1978; Veldhuis and Admiraal, 1989), and within diatom blooms, where silica may restrict diatom growth. Surface concentrations of nitrate above a stable thermocline can fall to G0.02 PM with very low standing stocks of phytoplankton (GO.1 mg chlorophyll a m-3). The summer reduction of nitrate and phosphate in surface stratified waters is largely balanced by increases in dissolved organic nitrogen and phosphorus (Butler et al., 1979). Only within dense phytoplankton blooms do concentrations of particulate nitrogen and phosphorus ever exceed those of dissolved forms. In regions of weak tidal mixing, levels of inorganic nutrients below the thermocline increase during the summer due to continued regeneration in deep water and the bottom sediments (e.g. Pingree et al., 1976; Morin et al., 1985). However, where tidal mixing is stronger and the thermocline less well developed, the upward fluxes of nitrate and phosphate balance or exceed rates of bottom regeneration. This effect promotes more efficient utilization of the nutrient stock within the water column, and provides an explanation for higher standing stocks of plankton in weakly stratified and frontal areas (Holligan, 1981); it may be further reinforced by spring-neap cycles of tidal mixing (Pingree et al., 1977a) and by the advection of nutrient-rich bottom water (Morin et al., 1985). During the summer, both in mixed and stratified waters, the available nitrate (and inorganic phosphate) for phytoplankton growth is supplemented by regeneration processes. More is known about the recycling of nitrogen, as standard methods have been developed for measuring the products of heterotrophic activity, such as ammonium, urea and amino acids, in sea water. However, no really consistent picture has yet emerged of the distributions and fluxes of these compounds. With the prevailing low concentrations in offshore waters, samples must be analysed immediately for reliable determinations and there are considerable experimental difficulties in estimating rates of turnover. There is evidence that ammonium (Foster et al., 1985; Q u S guiner et al., 1986), urea (Turley, 1986) and amino acids (Poulet et al., 1984; Williams and Poulet, 1986; Flynn and Butler, 1986) are all important sources of nitrogen for natural phytoplankton populations, and the addition of such compounds is known to stimulate photosynthetic rates (Davies and Sleep, 1981). On the other hand, attempts to estimate nitrogen requirements, together with observations on zooplankton excretion (Holligan et al., 1984b; Harris and Malej, 1986), indicate that most of the regenerated nitrogen is supplied as ammonium. In autumn, increased mixing across the thermocline, due to surface cooling and wind, enhances the supply of nutrients to the surface mixed layer. But

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the balance between this process and the maintenance of an adequate light regime (a combination of surface irradiance and stability) does not always allow the development of a well-defined autumn bloom. As a result, the timing and extent of increases in phytoplankton biomass at this time of year are irregular (e.g. Pingree et al., 1976). Although no detailed analysis of regional variations in nutrient distributions on the NW European shelf has been carried out, it is apparent that mixed, frontal and stratified waters are quite distinct in this respect (e.g. Savidge and Lennon, 1987). The underlying causes include variations in the depth of the mixed layer (or water column for unstratified waters), which define the initial nutrient input, and the relative importance of light and nutrients in controlling growth, as well as differences in mixing rates across the seasonal thermocline (see Holligan et af., 1984b), and the effects of advection, eutrophication and short-term regeneration (i.e. excluding winter regeneration) which determine nutrient supply during the summer period. Examples of seasonal changes are provided by Baeyens et af. (1 984) for inorganic nitrogen in the southern North Sea, and by Butler et al. (1979) and Wafar et al. (1983) for nutrients in stratified and mixed waters of the western English Channel. Regenerated nutrients tend to be relatively more important in surface stratified waters due to restricted renewal across the seasonal thermocline, although rates of regeneration can be higher in eutrophic inshore waters.

D. GRAZING

Herbivorous zooplankton, apart from acting as a source of regenerated nutrients, directly affect primary productivity whenever the grazing rate is significantly different from the phytoplankton growth rate. Cushing ( I 983) discusses the evidence for the control of plant production by herbivores based on the observation that the spring maximum in plant biomass is reached before the main decline in nutrient levels. There is also evidence to suggest that grazing lags behind primary production allowing a significant proportion of the phytoplankton to sink through the developing thermocline (Davies and Payne, 1984) and be consumed by benthic organisms (Fransz and Gieskes, 1984). The control of phytoplankton biomass by herbivory depends on an increase in the reproductive rate of the plant cells being matched by an increase in grazing rates due to reproductive strategies (e.g. Williams and Conway, 1984) or aggregation (Fransz and Diel, 1985) of the herbivores. However, once the water column is stratified the inorganic nutrients are depleted over a period of 1-4 weeks, depending on the stability of the thermocline, to uniformly low levels (e.g. Pingree er al., 1977b). This condition indicates that nutrient availability rather than grazing is the overall factor limiting primary

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production during the spring months. Subsequently a quasi-steady-state condition is reached, with nutrient input (renewal across the thermocline plus regeneration), phytoplankton growth and herbivory in balance with one another. The grazers are the dominant cause of algal mortality and provide a large proportion of the regenerated nutrients. Thus, the behaviour, feeding, growth and excretion of herbivores such as copepods (e.g. Williams and Conway, 1984; Daro, 1985; Die1 and Klein Breteler, 1986; Harris and Malej, 1986) influence both the growth (nutrient assimilation) and survival of phytoplankton cells. For the shelf waters of NW Europe the copepods are generally considered the dominant herbivores, with other groups such as protozoa (e.g. Admiraal and Venekamp, 1986) locally important. However, in surface stratified waters it appears from biomass distributions (Holligan et al., 1984a; Fogg rf al., 1985), from the abundance of small ( < 5 pm diameter) autotrophic cells which are not captured efficiently by copepods (Joint and Williams, 1985), and from grazing experiments (Burkill et al., 1987), that much of the grazing is by microheterotrophic organisms, including non-photosynthetic dinoflagellates (Jacobson and Anderson, 1986). It is still difficult to take proper account of these organisms in constructing carbon budgets for marine ecosystems due to the lack of information on rates of feeding and excretion within natural populations. This problem is well illustrated by attempts to define the role of bacteria. Although bacterial activity is found to be coupled to primary production and is important in remineralization processes (Lancelot, 1924; Lancelot and Billen, 1984; Lochte and Turley, 1985), there is much uncertainty about how much of the carbon flow to higher trophic levels is through bacteria. Observational data (Holligan et al., 1984b; Joint and Williams, 1985) indicate that microheterotrophic organisms are relatively unimportant for the food chain except through their contribution to remineralization, whereas theoretical considerations have led to the opposite viewpoint (Newell and Linley, 1984). Persistent blooms of dinoflagellates, in which increases in cell density over a period of several weeks are associated with relatively low abundances of herbivores (Lindahl and Heinroth, 1983; Holligan et al., 1984a), represent a special case. The combination of reduced grazing rates, perhaps due to some inhibitory effect and assimilation of nutrients from subthermocline water (Holligan et al., 1984b), lead to high phytoplankton biomasses, with the standing stocks of particulate carbon and nitrogen per unit area representing a relatively large proportion of annual primary production values.

E. ANNUAL PRODUCTION CYCLE

Various attempts have been made to summarize the observed changes in phytoplankton abundance and species composition in temperate marine ecosys-

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tems with respect to environmental conditions. A generalized scheme of events is shown in Fig. 9, based on the analysis of Bowman et al. (1981). Differences in light and nutrient availability, which are determined primarily by the timing of thermocline establishment and breakdown, cause a divergence in terms of phytoplankton growth rates and species succession. This effect is made clearly apparent by comparing seasonally stratified waters with those that remain well mixed throughout the year (e.g. Maddock et af., 1981). In regions adjacent to frontal boundaries where stratification develops late and is eroded early, the growth season may only be half as long as in areas of persistent seasonal stratification (see Pingree, 1975). In general, in the former situation there is a tendency for the summer flagellate communities to last a relatively short time and for the autumn diatom bloom to be more pronounced. In mixed water regions, depending on the depth and turbidity of the water column, kh values may be sufficiently large to allow only a weak diatom bloom in mid-summer, or, at the other extreme, low enough for the depletion of inorganic nutrients and the replacement of diatoms by other phytoplankton types. Significant year-to-year and longer term (Colebrook and Taylor, 1984; Radach, 1984) differences in phytoplankton distributions are also likely to occur in response to climatic variability which, through the effects of wind and solar radiation, determines the stability and light environment of the surface layer. The various seasonal patterns for phytoplankton abundance in the shelf waters of NW Europe, as illustrated in an idealized form in Fig. 10, reflect differences in kh values and in timing of thermocline formation and breakdown. There is considerable evidence both from field observations and from modelling work that these are representative of the range of shelf water environments.The main problem is to evaluate such distributional patterns in terms of net productivity. Statistical analyses (Jordan and Joint, 1984; Platt, 1986) suggest that, for a relatively restricted area where variations in annual insolation are small, biomass and productivity are correlated. However, regional and temporal differences in the vertical distribution of light and chlorophyll, in P-Z relationships, in carbon-nitrogen and carbon+hlorophyll ratios and in other properties determined by the species composition and age of populations indicate that such a simple relationship is unlikely. For example, within frontal dinoflagellate blooms, it appears that both net productivity per unit area and growth rate of the population decline as standing crop increases and self-shading leads to light limitation (Holligan et af., 1984b3.

V. EVALUATION OF PRIMARY PRODUCTIVITY ESTIMATES A. GENERAL CONSIDERATIONS

The main objective of marine primary productivity studies is to estimate net

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S D

3

2

1 I

I

I

10

1

0.1

I

kh 2-

4-

void

10 Fig. 9. Diagrammatic representation of the seasonal succession of phytoplankton in relation to changes in water column illumination, kh, and vertical stability, S. Although the sequence of events in space and time cannot be fully defined in terms of two parameters, realistic values for kh and S are indicated (see text for definition of terms). Note that kh is plotted on a logarithmic scale. An alternative measure of surface layer stability is shown by values for D,the vertical diffusivity across the pycnocline (cm2s-l). Modified from Bowman et al. (1981).

photosynthetic carbon fixation for the whole, or some defined part, of the annual cycle. Ideally, information on the production of dissolved as well as particulate organic carbon should be included. Furthermore, with respect to food chain dynamics, the efficiency with which different forms of plant carbon (i.e. large cells, small cells, dissolved material) is also of interest, although such details lie beyond the scope of this account. The nutrient budget approach to estimating primary productivity in shelf waters is based on standard, well-accepted ratios for carbon, nitrogen and phosphorus in plant material, on precise measurements of changes in nutrient concentrations in the water column, and on some objective assessment of nutrient recycling (e.g. Owens et al., 1986). Uncertainties in parameters such

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Shallow

Mixed

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2 1

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F

Fig. 10. Predicted annual changes in net primary productivity for different water types on the NW European shelf. S, spring outburst; DB, dinoflagellate bloom; A, autumn bloom. The vertical scale, although arbitrary, does indicate relative changes in rates of phytoplankton production.

as vertical diffusivity and vertical nutrient gradients, which are critical for more precise estimates of nutrient fluxes (e.g. Steele, 1956), can be corrected as improved observational data become available. Also, the significance of horizontal gradients in nutrient concentrations such as occur across frontal boundaries can be semi-quantitatively assessed (Loder and Platt, 1985). Essentially similar results are obtained from budgets for phosphorus or nitrogen, although those for nitrogen have received greater attention in recent years as regeneration processes have become better understood. Few detailed nutrient budgets have been prepared for the shelf waters of NW Europe. However, they are of particular importance as they consider phytoplankton growth over extended time periods (e.g. an annual cycle), and also take into account spatial variations in the basic physical and chemical

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properties of the water column. Also they are fully compatible with ecological models in which nutrients and light are the forcing functions (Tett et al., 1986; Taylor et al., 1986). By contrast, measurements of photosynthetic carbon fixation using the I4C method, which represent the main source of information on primary productivity, are difficult to interpret with respect both to the distinction between net and gross production and to the problems of extrapolation from the results of short-term experiments (often < 6-h incubation periods) to daily or longer-term production rates. Furthermore, 14C02 fixation experiments effectively provide only point values which, for practical reasons, cannot be obtained with sufficient frequency to allow a realistic appraisal of temporal and spatial variability in the primary productivity of heterogeneous physical environments such as the NW European shelf region. For this reason, particular care must be taken to check that experimental incubations are carried out under a representative range of light conditions, and that subsurface features such as chlorophyll maxima are adequately sampled. As emphasized by Platt and Harrison (1985), as much attention should be given to variances as to means in considering the overall dynamics of the growth of natural phytoplankton populations. The main value of 14C02uptake experiments has been in examining particular features of the growth characteristics of phytoplankton, such as the effects of light and nutrient levels on photosynthetic rates, the exudation (excretion) of organic carbon, and the relationship between biomass and potential productivity. Net productivity values based on the I4C method alone depend on some explicit correction for or assumption about plant respiration. If the activity of heterotrophic organisms is relatively slight, 24-h incubations with I4CO2may provide a direct measure of net photosynthesis or, alternatively, corrections for respiration can be made by comparing I4CO2 uptake rates in the light with the results of parallel measurements of light and dark changes in oxygen, of nutrient uptake and of pH shifts. However, in reviewing the published data, it is apparent that such supplementary information is generally unavailable. ,Most 14C02productivity estimates deal only with particulate organic carbon. Mainly for methodological reasons, there are still relatively few reliable measurements of exudation that can be considered relevant to natural situations. On the whole they indicate exudation rates of about 10% of total carbon fixation, although it is difficult to take into account possible reassimilation of organic matter by the plant cells, as shown recently for Phaeocystis colonies (Veldhuis and Admiraal, 1989, or by heterotrophs. The ecological significance of phytoplankton exudation therefore remains uncertain. Regardless of method, any overall assessment of primary productivity in NW European shelf waters must also deal with a major inconsistency in the interpretation of observational data; certain estimates of plant production

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(e.g. Steele, 1956) continue to be accepted as representative of the whole shelf ecosystem, whereas advances in understanding the effects of physical mixing processes on the environmental conditions for phytoplankton growth (Pingree, 1980) indicate that regional variations in annual productivity are considerable. Although there is increasing evidence from comparative studies at different sites for such regional variability (e.g. Gieskes and Kraay, 1984), objective methods for defining or predicting the range of annual production values have yet to be established. B. MIXED WATERS

Strong tides maintain well-mixed water conditions during the summer months in much of the Irish Sea, the southern North Sea, and the eastern English Channel extending westwards along the coast of NW France (Fig. 7). In these regions the combined effects of variations in depth and turbidity (i.e. kh) lead to a wide range of primary productivity values; for example, 20-fold differences in annual (gross) rates have been reported for the Bristol Channel (Joint and Pomroy, 1981). However, rates of net production are difficult to establish, partly because phytoplankton respiratory losses can be a high proportion of gross photosynthetic fixation, leading to large potential errors in estimates of the small differences between the two, and partly because the rates of nutrient inputs from rivers and from regeneration processes in the water column and sediments are hard to assess. A further problem is that changes in irradiance experienced by the plant cells as a result of vertical motion are not easy to simulate in a productivity experiment, leading to possible errors in the parameterization of the P-I curve, except when the timescale of mixing is too short to allow photoadaptive responses (Uncles and Joint, 1983). The most detailed investigations of phytoplankton growth in mixed waters have been undertaken off the Belgian coast. A recent summary (Joiris et al., 1982) gives a value of 320 g C m-2 yr-l, based on measurements by the 14C02 method, for total net primary production of which 60% is in a particulate form. However, it is not clear how corrections were made for phytoplankton respiration. A major discrepancy between carbon and oxygen fluxes is interpreted as evidence for rates of gross primary production up to 2000 g C m-2 yr-I, a much higher value than has been reported for other areas. Other I4C estimates of particulate primary production are > 300 g C m-2 yr-' in coastal waters off NW France (Wafar et al., 1983) 200-250 g C m-2 yr-l in the Southern Bight (see Fransz and Gieskes, 1984), about 140 g C m-* yr-l in mixed waters of the western English Channel (Boalch et al., 1978), and 7-165 g C m-2 yr-' in the Bristol Channel (Joint and Pomroy, 1981). These data cannot be compared directly, owing to different sampling and experimental procedures, but there is evidence from separate areas for a positive correlation between chlorophyll concentration and the rate of primary

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productivity. The effects of turbidity and water depth on productivity are clearly demonstrated (e.g. Joint and Pomroy, 1981), and there is general agreement between various estimates of daily and seasonal productivity for the southern North Sea (Gieskes and Kraay, 1975,1977; Lancelot and Billen, 1984; Veldhuis et al., 1986b), with the highest values for the less turbid offshore waters. Rates of exudation are very variable, but are commonly 10% of total production even in the presence of mucilaginous colonies of Phaeocystis (Joint and Pomroy, 1981; Veldhuis et af., 1986a). Hydrographic data for the Southern North Sea (Brockmann and Wegner, 1985) and eastern English Channel (Holligan ef af., 1978) show that the spring phytoplankton bloom may begin locally as early as February, and a winter nutrient minimum over the Dogger Bank is indicative of net growth of the phytoplankton throughout the winter (Postma, 1978). However, both for these regions and for the Irish Sea, no annual estimates of primary production appear to be available even though seasonal studies of I4CO2fixation have been undertaken (Gros and Ryckaert, 1983). A model for phytoplankton growth at a mixed water station in the central English Channel (Agoumi et al., 1985) gives a gross productivity value of 35 g C m-z yr-I, which seems unrealistically low. Brander and Dickson (1984) have suggested that low levels of fish production in the Irish Sea may be related to a short phytoplankton growth season and low annual productivity. A mean irradiance level of about 0.03 cal cm-' day-' is required to allow positive net production in a mixed water column (see Gieskes and Kraay, 1975; Pingree et al., 1976), and increases in phytoplankton biomass occur once this value is exceeded. However, changes in species composition (Maddock et af.,1981) are observed when no net production is predicted, perhaps as a result of temporary relaxation in vertical mixing at times of sunshine, low wind speeds and neap tides. Exceptionally early blooms can also develop (Boalch et af., 1978; Reid et af., 1983) in association with strong river outflows, and these may be an important source of variability in annual productivity. It is important to note that gross production will always be measurable in winter (Fransz and Gieskes, 1984) as long as there is phytoplankton in the water, but will largely be dissimilated by respiration. The mixed water regions of the NW European shelf are affected by nutrient inputs from the major rivers, and are therefore likely to show changes in productivity as a result of hypernutrification. There is little direct evidence for this hypothesis . However, Postma (1978) suggests that there may have been a 20-40% increase in primary production in the southern North Sea over the last few decades, and that the widespread Phaeocystis blooms in the spring may be the result of higher inputs of nitrogen and phosphorus as opposed to silicon, a lack of which now restricts diatom growth. The increase in abundance of Phaeocystis at the entrance to the Wadden Sea has been documented by Cadee and Hegeman (1986), and nutrient models for Dutch coastal waters indicate a doubling of primary production between 1930 and

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1980 (Fransz and Verhagen, 1985). Wafar et af. (1983) report substantial increases in annual mean and daily maximum production values in Morlaix Bay (NW France) between 1966 and 1986 which they ascribe to increases in available nitrogen.

C. STRATIFIED WATERS

Over most of the NW European shelf the water column is stratified during the summer months (Fig. 7), with the thermocline becoming established in April and May and persisting in areas of weak tidal mixing until early winter (e.g. Pingree, 1975). The first detailed estimates of net primary production were made by Steele (1956) for the northern North Sea from an analysis of 3 years’ data on phosphate distributions. The annual values ranged between 54 and 127 g C m - 2 yr-l, being lowest in offshore areas where vertical mixing is weak in the summer and highest in inshore waters off NE Scotland. One uncertainty in the calculations concerned the rate of phosphate regeneration in the surface layer, and the assumption that this is not zero but the same as in the bottom layer increased the productivity estimates by 25-33%. Also, considerable differences between the years were apparent, due mainly to variations in vertical mixing in the summer and autumn. Almost all subsequent models of the North Sea food chain have used an average net primary production rate of 100 g C m-? yr-I based on Steele’s work (e.g. Jones, 1984). Another phosphate-based production budget for Station E l in the western English Channel was described by Pingree and Pennycuick (1975). In this case the temperature and nutrient data were the averages of many years observations. For a shallower water column than the northern North Sea and lower winter maximum phosphate levels, the annual production was again calculated to be about 100 g C m-* yr-’, with about one-quarter attributable to the seasonal reduction in ambient dissolved inorganic phosphate and the remainder to recycling processes. Regeneration rates were estimated for the bottom mixed layer and assumed to be uniform through the whole water column. In both these studies water bottle sampling at 10-m intervals did not allow the gradients in phosphate across the thermocline to be accurately defined. Using a continuous pump sampling technique, Holligan et af. (1984b) showed that vertical distributions of nitrate are strongly modified by uptake in the subsurface chlorophyll maximum, and that under extreme conditions within a dinoflagellate bloom the change between surface and bottom layers is confined to the very base of the thermocline. For a given mixing rate, the upward flux of nutrient will be proportional to the nutrient gradient, which may vary by more than an order of magnitude (Holligan et al., 1984b). Thus the earlier estimates of net primary production rates in stratified waters based

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on vertical phosphate fluxes must be considered as minimal values, especially as a faster removal of phosphate from bottom water associated with a steeper vertical gradient in concentration would also imply more rapid rate of regeneration. Steele (1957a,b) showed that dissolved oxygen measurements and the results of a few I4Cexperiments supported the phosphate productivity estimates. Since then the only intensive study of primary production in the northern North Sea has been the FLEX study in the spring of 1976. From a comparison of methods based on pH changes, nutrient uptake and I4C uptake, net carbon fixation between the end of April and beginning of June was about 30 g C m-2 (see Weichart, 1980). This approach has yet to be applied to the full annual cycle. For other areas of stratified water, annual production values based on the 14Cmethod are -250 g C m-2 yr-' in the central North Sea (Gieskes and Kraay, 1980), 180 g C m-2 yr-l in the western English Channel (Russell et af., 1971; Boalch et af., 1978), and 100 g C m-2 yr-I in the Celtic Sea (Joint et al., 1986) and in Norwegian fjords (Erga and Heimdal, 1984; Eilertson and Tasen, 1984). However, these figures are not really compatible, being based on different ways of distinguishing net and gross primary production and on different sampling strategies. Furthermore, for a single location, Station E 1 off Plymouth, a measure of the uncertainty is given by the range of published values (all g C m-'yr-'): 180 from l4Cexperiments (Russell et al., 1971), 100 from a phosphate budget (Pingree and Pennycuick, 1975), and 70 from a model of phytoplankton growth (Agoumi et al., 1985). It seems likely that the average net annual primary productivity at this station is between the first two values. A model for a similar site in the west central North Sea also gave an anomalously low net production value of 37 g C m-2 yr-' (Horwood, 1982), although this figure was considered reasonable in terms of relatively low winter nutrient concentrations and a shallow mixed layer in summer. Other I4C data for phytoplankton productivity in stratified waters relate mainly to daily rates at particular stations. Most measurements are for midsummer, when the phytoplankton biomass is relatively low and growth is supported mainly by nutrient regeneration. Daily fluctuations in production rates are considerable (e.g. Joint and Pomroy, 1983), reflecting variations in irradiance and perhaps in the species composition and physiological properties of the phytoplankton (Joint and Pomroy, 1986), but mean values may be a reasonable approximation of net productivity under conditions of relatively small respiratory losses. Rates of about 0.5 g C m-2 day-' appear to be typical (Joint and Pomroy, 1983; Holligan et af., 1984b; Joint et al., 1986), but rates tend to be higher close to frontal zones (Jordan and Joint, 1984; Gieskes and Kraay, 1984) and lower in the most strongly stratified water (Steele, 1957a). The seasonal thermocline persists for several months over a large propor-

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tion of the NW European shelf (Fig. 7). For this reason, low-nutrient stratified waters, although exhibiting relatively low daily rates of production, make a substantial contribution to total annual productivity. Some assessment of range and va,riability in production rates in such waters is therefore required. At two stations in the western English Channel, Holligan et al. (1984b) estimated upward fluxes of nitrate to be 5.74 and 3.22 pg nitrate nitrogen cm-2 day-'. A similar calculation for the region of strong stratification of the north central Celtic Sea, based on the hydrographic data of Pingree et al. (1976), gives < 0.5 pg nitrate nitrogen cm-* day-' assuming that a subsurface chlorophyll maximum is present within the thermocline. Although this order of magnitude difference may be partially offset by more efficient recycling of nutrients at the more oligotrophic station, it does suggest large regional variations in summer production rates even in waters unaffected by frontal blooms (see following section). A similar conclusion is drawn from observations of pH distributions in the German Bight (Weichart, 1985) which indicate primary production values 2-3 times those of the open North Sea. As pointed out by Steele (1956), relatively little is known about primary production in the autumn. Seasonal studies of biomass (Reid, 1978; Holligan and Harbour, 1977) and productivity (Boalch et af., 1978) show increases at this time of year, but the autumn outburst remains a somewhat enigmatic event in terms of its overall contribution to annual productivity, especially as much of the organic carbon may be subsequently lost through phytoplankton respiration as the water column becomes well mixed. On the other hand, in regions such as the central North Sea it may be as important as the spring bloom (Cushing, 1983).

D. FRONTAL REGIONS

Rates of primary productivity are least well documented for frontal regions between well-mixed and seasonally stratified waters (Fig. 7), partly because their biological significance has only recently been recognized, and partly because the problems of sampling within a complex physical environment are considerable. Furthermore, although tidal fronts often show relatively high standing stocks of phytoplankton, there are strongly divergent opinions as to what these signify in terms of biological production processes. The physical properties of frontal boundaries are variable with respect to cross-frontal gradients in density, spring-to-neap differences in tidal streams, water depth, along-frontal advective flow, cross-frontal instabilities (i.e. eddies) and exchange etc. Biological properties also vary, both spatially and temporally, within any frontal region and between different fronts, as is well illustrated by surveys (Pingree et al., 1978; Savidge and Foster, 1978) and seasonal studies (Holligan, 1981; Richardson et al., 1985) of phytoplankton

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distributions. During the summer months at least three patterns can be recognized (see also Fig. 10): 1. Deep ( > 60 m) water fronts where nutrients remain relatively high in both mixed and subthermocline waters, and maximum chlorophyll concentrations are at the front boundary and extend into the shallow thermocline (Pingree et al., 1982). 2. Shallow ( < 60 m) water fronts where the main horizontal temeprature gradients are in the bottom water, nutrient levels are generally low. and chlorophyll maxima can be displaced to the stratified side of the frontal boundary (Creutzberg, 1985). 3. Localized fronts for which the length scale of the boundary is relatively small compared to the rate of along-frontal advection so that any increase in chlorophyll due to growth is masked by dispersion within surrounding waters (Jones et al., 1984). Intermediate situations are also found, especially in shallow waters where the balance between light and nutrient effects on phytoplankton growth is strongly influenced by varying weather conditions (sunlight, wind mixing). There is no time series of primary productivity measurements for a single frontal region, although comparative observations on frontal, stratified and mixed waters have been made (Fogg et al., 1985). For conditions where the bloom dinoflagellate, Gyrodinium aureolum, has been absent, higher rates of photosynthetic carbon fixation have been found close to the front compared to well-stratified waters (Richardson, 1985; Richardson et al., 1986; Videau, 1987), with maximum values up to 1.8 C m-2 day-'. In the latter two studies, no significant differences in rates of primary productivity were found between frontal and well-mixed stations, but the possibility of relatively high losses of carbon in the mixed waters due to dark respiration were not considered (see Holligan et a[., 1984b). Most other production measurements in frontal regions relate to blooms of G . aureolum (see Partensky and Sournia, 1986). For thermocline and early bloom populations, maximum rates of photsynthesis (P,,J are in the range 5-log C (g Chl a)-' h - ' (Pingree et al., 1976; Holligan and Harbour, 1977; Jordan and Joint, 1984; Tett et al., 1986), which are similar to those for other phytoplankton species. By contrast, within frontal blooms (Chl a >20 mg m-3), the water column becomes depleted of inorganic nutrients, values for P,,, are < 1 g C (g Chl a)-' h-I, and the population growth rate is close to zero (Holligan et al., 1984b). It appears, therefore, that nutrient depletion leads to reduced photosynthetic efficiency and a lower growth rate. Survival of the bloom must also depend on low grazing mortality. These effects, together with the vertical distribution of G . aureolum which enable the sequestration of nutrients from bottom water (Holligan et al., 1984b), provide a mechanistic explanation for the exceptional blooms of this dinoflagellate along tidal fronts (Pingree et al., 1975). The standing crop of G . aureo-

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lum can exceed 50 g C m-* (Holligan et al., 1984a), which represents a real minimal value for net primary production, assuming no horizontal accumulation (see below). Satellite observations suggest that large blooms develop in about 1 month (Holligan et al., 1983a) so that maximum rates of net photosynthesis are likely to exceed 2 g C m2-' day-' in the early stages. Indirect evidence for high rates of primary production in frontal regions comes from a consideration of the relationship between chlorophyll standing crop and photosynthetic rate. Despite the variability in photosynthetic parameters (Savidge and Foster, 1978; Videau, 1987), there is evidence for a positive correlation between biomass and production rate in stratified and frontal waters (Richardson, 1985; Videau, 1987), with daily primary productivity being determined largely by surface irradiance (Jordan and Joint, 1984; Platt, 1986). In view of the sampling problems for rate measurements, determining the distributions of chlorophyll and of optical properties may prove to be the most useful approach to assessing primary productivity in frontal regions, with blooms of dinoflagellates such as G. aureolum being treated as a special case. The inference that the high chlorophyll concentrations commonly observed at tidal fronts are indicative of high rates of production has been questioned by Le Fevre (1986), mainly on the grounds that physical aggregation within convergent circulation patterns is a more likely explanation than in situ growth. Physical accumulation mechanisms are known to be important over scales of 1 km or 1 day (Mackas et al., 1985), as is clearly evident from direct observations in frontal regions (Pingree et al., 1975). However, at scales of 1 &I 00 km (days) characteristic of the frontal blooms, biological properties (i.e. growth) are almost certainly dominant in determining phytoplankton distributions and abundance. Within the blooms, local accumulation effects associated with Langmuir cells, internal waves etc. are usually observed. Le Ftvre (1986) is also critical of the use of one-dimensional vertical models and concepts to explain algal growth in complex physical environments such as frontal regions. In both observational (Pingree et al., 1975; Holligan et al., 1984b) and modelling (Tett et al., 1986) work, this approach to considering light and nutrient availability was adopted as the best practical means for understanding phytoplankton growth in frontal ecosystems. The assumption that vertical mixing processes are, in general, more important than horizontal ones in determining nutrient fluxes is substantiated by theoretical considerations (Loder and Platt, 1985). Furthermore, no rational hypotheses based on horizontal mixing and advection to explain nutrient and chlorophyll distributions in both deep and shallow water fronts (Pingree et al., 1978) have yet been formulated. E. SPATIAL AND TEMPORAL VARIABILITY

Within the main types of physical environment on the continental shelf-

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stratified, frontal and well-mixed waters (Fig. 7)-the environmental factors that control phytoplankton growth are extremely complex. For this reason alone, it is not surprising that the range of estimates for annual primary productivity appears to be considerable, both spatially (Steele, 1956; Fransz and Gieskes, 1984) and temporally (Russell et al., 1971). The causes are both direct and indirect influences on nutrient and light availability, including the effects of wind, precipitation, river run-off and surface heat fluxes on stratification, the effects of river run-off and shelf break exchanges on nutrient levels, and the effects of sunshine and turbidity (coastal erosion, bottom mixing, rivers, etc.) on water column irradiance. For any given location, annual differences in primary production are likely to be related largely to the light environment; a more efficient utilization of nutrients, and therefore higher productivity, will result from above-average solar illumination (especially with respect to photosynthesis in mixed water columns and within the thermocline) and from longer-than-average periods of stratification. By contrast, the initial (late winter) nutrient content of the water column is rather constant (Pingree et al., 1977b) from year to year, so that differences in nutrient availability are likely to be relatively small. Blooms of the dinoflagellate Gyrodinium aureolum, within which a high nutrient input of nutrients across the seasonal thermocline is maintained by biological processes (Holligan et al., 1984b), are exceptional in this respect. The ecological significance of variations in primary productivity has not been investigated in any detail except through modelling work (e.g. Steele, 1974), although it is recognized that certain shelf areas are characterized by greater secondary productivity than others (Brander and Dickson, 1984). In particular, annual variability within a given region is poorly understood, in terms of both the relative magnitude of the effect and how it influences the food chain. This seems a rather intractable problem due to the difficulties of adequate sampling and of making appropriate rate measurements.

VI. FATE OF PLANT MATERIAL WITHIN THE SHELF ECOSYSTEM Most of the uncertainty in values of net primary production for NW European shelf seas arises from various sampling and methodological problems. Attempts to evaluate the fate of plant material in the ecosystem have led to similar doubts about the quantities of organic material produced. Such studies have ecological or biogeochemical objectives, and often include measurements of properties that relate to population taxonomy (cell size, sinking rates, pigment composition, mineral phases, storage products, etc.). There are two main conclusions from the ecological work. Firstly, in a reevaluation of Steele’s (1974) model of the North Sea food chain, Baars and

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Fransz (1984) estimated that the accepted value for phytoplankton production (-90 g C m-2 yr-I) is low by a factor of about two. This view stems partly from a consideration of new information on the energy requirements of benthic (see Wilde et al., 1986) and microheterotrophic (see Burkill et al., 1987) organisms, and partly from restrictions imposed by more realistic models of the relationship between photosynthesis and fish production (Jones, 1984). It is now recognized that the Fladen Ground in the northern North Sea, where Steele made his detailed observations on primary production, is an area of relatively low biological activity due to the prevailing physicochemical conditions in summer. But, remarkably, comparable nutrient budgets have not been undertaken for other hydrographically distinct regions of the continental shelf. There is increasing evidence for the sedimentation of a substantial proportion of the phytoplankton standing crop each year. As pointed out by Fransz and Gieskes ( 1984), conditions when the phytoplankton growth rate exceeds the zooplankton grazing rate occur regularly, and will normally result in the loss of plant material to the bottom water and sediments. This imbalance may be due either to rapid phytoplankton growth, as at the time of the spring diatom outburst, or to some inhibition of grazing as occurs within populations of colonial flagellates such as Phaeocystis (Joint and Pomroy, 1981; Joiris et al., 1982) and of dinoflagellates (e.g. Holligan et al., 1984a). Vertical fluxes of particulate material are difficult to measure in waters stirred by tides, but sediment traps have shown that large quantities of plant material do sink through the seasonal thermocline (Davies and Payne, 1984; Cadee, 1985, 1986b). Furthermore, on a larger scale, there is speculation that substantial amounts of phytodetritus may be transported from continental shelves to the continental slope (see Rowe et al., 1986). This scenario has yet to be critically examined for the NW European shelf, but the Norwegian Channel is known to be a major sink for particulate material from the North Sea (van Weering, 1981). The second ecological conclusion is that there are consistent spatial variations in primary production rates which, for the main part, are attributable to physical mixing processes and the disposition of tidal fronts. This is based on studies of larval fish (see Sinclair and Tremblay, 1984), planktonic organisms (e.g. Kisrboe and Johansen, 1986) and benthic animals (e.g. Creutzberg, 1985). In each case variations in total biomass of consumer organisms are usually associated with changes in species composition so that, on account of differences in growth efficiencies for individual species, it is not possible to relate heterotroph biomass to autotroph productivity directly. However, physiological evidence, such as that presented by Moal el al. (1985) on digestive enzyme activity in zooplankton, should resolve this problem of interpretation. The biogeochemical investigations (e.g. Lancelot et al., 1986) are less well advanced in providing quantitative information, relative or absolute, about

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rates of primary productivity. However, the types and proportions of plant products, which vary with growth conditions as well as taxonomic composition (Morris, 1981), include specific compounds that can be monitored in secondary (i.e. after death or predation) dissolved and particulate phases. Substances resistant to microbial degradation and chemical dissolution are of particular interest in this context. Examples from sediments include silica frustules of diatoms, calcite coccoliths (plates) of coccolithophores, plant pigment and their degradation products (e.g. Billett ef af., 1983), fatty acids attributable to diatoms (Smith et af., 1983b), dinoflagellate sterols (Boon et af., 1979), and coccolithophore longchain ketones (Brassell et al., 1986). In each case relative information on rates of primary production can be inferred from deposition rates and from taxonomic data-for example, diatom remains are indicative of more productive ecosystems than dinoflagellate or coccolithophore remains, at least for oceanic ecosystems (see Margalef, 1978). The dissolved products of phytoplankton metabolism are less well known due to analytical difficulties, but trace volatile substances which can be isolated from sea water and concentrated are likely also to prove valuable in this context. For example, the distribution of dimethyl sulphide, a cleavage product of the osmolyte dimethylsulphoniopropionate,is an indicator of certain types of phytoplankton (Holligan er al., 1987)and of grazing activity (Dacey and Wakeham, 1986). These marker compounds, even though they constitute only a small proportion of the total organic matter of phytoplankton, are likely to yield valuable information about variations in rates of primary production as conditions controlling their production and fate become better understood. For particulate organic matter in shelf seas affected by tidal stirring, there will always be special problems in interpreting distributional data due to the effects of resuspension. However, at least over short time-scales (i.e. days to weeks), studies on the dissolved products of phytoplankton metabolism, including volatile substances, are likely to provide important new information about the dynamics of phytoplankton growth.

VII. CONCLUSIONS Reliable estimates of the productivity of marine phytoplankton are required on a global scale for biogeochemical studies on the exchanges of materials between the ocean, atmosphere and marine sediments which play such an important role in determining the nature and stability of the global environment (Lovelock, 1986), and on a regional scale for the proper management of biological resources in coastal seas, which includes the need to predict the effects of over-exploitation and pollution on the food chain. Two basic questions arise: what controls phytoplankton growth, and what are the fluxes of materials through phytoplankton?

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For the shelf seas in general, including those of NW Europe, there has been considerable progress with the first question over the last 10-20 years. This has largely been the outcome of laboratory studies on phytoplankton growth and of field studies relating phytoplankton distributions to physical and chemical conditions in the water column. As a result, a more rigorous and objective framework has been given to the classical ecological studies completed during the first part of this century, and much of the variability in phytoplankton biomass can be explained objectively in terms of the effects of nutrients, light and grazing on species growth and succession. By contrast, progress with the second question has been slow. Estimates of net primary production for the NW European shelf are mainly in the range 50-300 g C m-? yr-’, and are based on various methods and assumptions. Although there is some consistency in the results, with the lower values for strongly stratified or highly turbid waters and with a degree of compatibility between different sets of observations, a rational analysis of either spatial variability in mean annual net primary production or of annual variability for a given location is still not possible. Thus for practical purposes there appears to have been little advance since the pioneering work of Steele (1956), with the exception of a better understanding of phytoplankton growth in coastal water areas as a result of multidisciplinary investigations (e.g. Joiris et al., 1982). There seem to be two reasons for this situation. First, far too much reliance has been placed on a single investigative method, incubation experiments with I4CO2, that gives results which are difficult to interpret in a physiological sense (i.e. the distinction between gross and net photosynthesis) and from which there is no dependable way to extrapolate in space and time. Secondly, biologists have made little use so far of new information about physical mixing processes in tidally stirred shelf seas. The latter is particularly surprising since Steele’s original computations depended on the parameterization of nutrient fluxes due to mixing across the seasonal thermocline and, furthermore, the results of 14C02and O2 measurements were used to check the validity of the phosphate production model. A fresh start therefore seems necessary, which not only incorporates recent concepts about nutrient regeneration and fluxes across the seasonal thermocline (the importance of both processes was clearly stated by Steele), but also makes use of the physical framework provided by tidal mixing models (Pingree, 1978b). Although the significance of the frontal boundaries in relation to plankton productivity remains controversial (Le Fevre, 1986) they d o represent predictable boundaries to distinct plankton communities in mixed and stratified shelf waters which have quite different, but as yet poorly defined, dynamic properties. In ecological terms, various causes of variability in plankton distributions are recognized. Climate has profound effects on the availability of light and nutrients to phytoplankton. In both mixed and stratified waters of the NW European shelf, significant annual differences (e.g. Maddock et al., 1981) and

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longer term trends (Reid, 1978; Robinson and Hunt, 1986) are found in both the species composition and total abundance of natural populations. Various hypotheses to explain the trends in relation to climate have been proposed (Southward, 1980; Radach, 1984; Colebrook and Taylor, 1984; Colebrook, 1986). Even more intriguing is the possibility of feedback effects on climate due to the release of volatile organic compounds by phytoplankton (Charlson et al., 1987). There are also changes due to human activities, particularly in response to nutrient discharges from rivers (Postma, 1978, 1985; Radach and Berg, 1986). In coastal waters, at least, these have affected phytoplankton distributions (Hickel et af. 1986) and led to increases in primary productivity (Cadee, 1986a). Against this background of variation and change, what is the best way of obtaining a more reliable and definitive account of primary production for the NE European shelf seas? “Baseline” studies based on restricted sets of observations using a single method such as I4CO2uptake will never suffice. One possible approach is through experimental ecophysiological work on the dominant species/taxa in the annual succession to define growth requirements and characteristics, in parallel with the development of rational models of phytoplankton productivity for realistic ecological (Fasham, 1985) and environmental (Taylor et al., 1986) situations. A combination of observational (including remote sensing) and experimental (using various methods) work at sea over appropriate time- and space-scales would allow the models to be objectively evaluated. However, for various practical reasons, a more effective approach is likely to be an extension of the nutrient budget method of Steele (1956) to include mixed and frontal, as well as stratified, waters. Nutrient analyses, giving continuous profiles (vertical and horizontal) of phosphate and nitrate, can now be used routinely on ships. Furthermore, with new information about the determinant physical, chemical and biological processes, rates of nutrient regeneration in the water column and sediments, and of nutrient exchange at boundaries (thermocline and fronts, as well as land-sea and sea-sediment interfaces) can be estimated more reliably. Specific problems such as the turnover of dissolved organic material or variations in the chemical composition of growing cells can be investigated experimentally. Also, as shown clearly by Steele (1956), the general problem of interannual variability appears tractable from a consideration of vertical mixing, although in a broader geographical framework the significance of horizontal advective fluxes may prove difficult to assess. It will not be an easy task to make a reliable and accurate description of phytoplankton productivity in the shelf seas of NW Europe, but the benefits for management problems and predictive purposes relating to future uses of these seas would be very considerable.

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AUTHOR INDEX

A Abbot, M . R.. 244,248 Abdullah, 71 Abreu-Grobois. F. A,, 19.48 Adair. W . S.. 56. 88 Adams, A. B.. 172. 173. 185 Adams. V. D.. 172. 173. 185 Adam. Y.. 248 Aderkas, P., von. 75.93 Admiraal, W., 224, 226, 230. 243. 251 Agoumi. A,. 21 7.232.234.243 Ahmed. S. I.. 244 Aiken. J . . 200. 243. 246. 250, 251 Al Araji. Z. T.. I7,48 Aldrich. H. C.. 67. 88 Alizai. S. A. K.. 145. 188 Allen. G. P.. 145, 185 Allen, J. R. L.. 104. 126, 129. 142, 143. I85 Allison, P. A., 142, 185 Alvin, K . L.. 176. 185 Ambard-Bretteville. F., 52 Amos, D. H.. 178. 187 Andersen, K . P., 194, 25 I Anderson, D. M . . 226.246 Anderson, J . A. R., 150, 185, 186 Anderson. R., 10, 31.48, 50 Anderson, A,, 123, 186 Anderson, E., 67,88 Anderson-Kotto. I., 87, 88 Andreae, M. O . ,243 Appleby, R. S., 10, 12, 51 Araki, S., 32, 34, 48, 50 Arao, T., 34,35,48,50 Arnold, M. K., 131, 188 Ashton, N. W., 90 Auling, G., 35,48 Austin, R. W., 203,243 Axelrod, D. I., 151, 186 Azarn, F., 21 1.243

253

B Baars. M . A,, 238,243.245 Baasch. K . H.. 52 Baeyens, W., 225,243.248 Bailay, R . W.. 92 Bajon-Barbier, C.. 60, 88 Baldwin, M., 72, 77,91 Bannister. T. T., 208. 209,247 Banse, K . . 197, 217, 243 Barber. J., 49 Barbier. C.. 60, 88 Barghorn, E. S.. 177, I88 Barmeier. J . C.. 189 Barrnett. R. J.. 45.46.47. 50, 51 Bartels, C. T., 44,48 Basaraba, J., I86 Bashe, D., 93 Bauer, L., 73, 74, 75, 88 Bearce, S. C., 187 Beardall, J., 194. 204, 245,249 Beck, J. C., 45.48 Bednara, J . , 69,92 Bell, E., 89 Bell, P. R., 59-93 passim Bellan, I., 200, 243 Beltz, C. K.. 68,90 Ben-Amotz. A., 47,48,49 Bennekom, A. J. van, 194,251 Benninghoff, W. S.. 108, 187 Benoit, R. E., 122. 186 Benson. A. A,, 2, 13.45,48,49 Bentley. D., 243 Berg. J., 242, 249 Berguis. E. M., 251 Berkaloff, C., 48 Berman, F., 248 Berman, T., 244 Berner, P., 250 Berrie, G. K., 75,89 Berry, E. W., 128, 186

254

AUTHOR INDEX

Bertels, A,, 214, 247 Berthois, L., 121, 186 Bessereau, G., 187 Bhardwaja, T. N., 71.89 Bhatnagar, A. K., 64,69,90 Bhatnagar, S. P., 63, 67.90,91 Billen, G., 226. 232, 247 Billett, D. S. M., 210, 240, 243 Billyard, T. C.. 48 Binelli, G., 92 Bird, E. C. F., 143, I86 Bird, J., 92 Birrien, J. L., 251 Bishop, D. G., 50 Bisseret, P., 48 Blasco, D., 209,243 Blecker, H . H., 50 Bligny, R., 52 Bloch, K., 50 Block, R. J., 10,49 Boalch, G. T., 197, 231, 232. 234,235, 243,248 Bolton, P., 7,48 Bonnevie-Svendsen, C., 99, 186 Boon, J. J., 240,243 Borowitzka, L. J., 20,48 Boschetti, A,, 10,49, 5 I Bose, A., 246 Bossard, P., 250 Bossicart, M., 247 Botkin, D. B., 252 Bowen, C. C., 90 Bowers, D. C., 219,250 Bowman, M. J., 222,227,228.243 Braarud, T., 197,243 Brack-Haynes, S. D., 177, 186 Braithwaite, A. F., 71, 89 Brander, K . M., 194,232,238,243 Brassell, S. C., 240, 243 Braten, T., 58, 89 Brawley, S. H., 58, 59, 89 Bray, J . R., 99, 186 Bredemeijer, G., 186 Bressler, S. L., 244 Brett, D. W., 189 Breuer, J., 51 Brewer, P. J., 215,243 Bridge, J . S., 126, 186 Broadwater, S. T., 59,65,89 Brockmann, U . H., 223,232,243 Broenkow, W. W., 245 Brown, A. D., 20,48 Brown, A. E., 4, 10,33,48

Brown, B. O., 245 Brown, J. W.. 245 Brown, R. C., 65,89 Bryan, G. S., 64, 89 Bryan, G. W., 40.48, 53 Bryan, J. R.. 213. 243, 251 Bryce, T. A., 9.48 Brylinski, J . M . . 222. 243 Burgeff, H . , 75. 89 Burkill. P. H., 226, 239, 243. 248 Burnham. R. J., 105. 128. 167. 168. 181. 183, 186. 190 Burris, J . E.. 204. 243 Burris, N., 53 Bustin, R. M., 143, 145, 146. 190 Butler, E. I . , 206. 207,224. 225, 243, 245. 249,250 Butler, R. D., 59. 92

C Cadee, G . C.. 232.239.242.243 Callow, J . A,, 90 Callow, M. E.. 90 Camefort, H., 64. 89 Campbell, J. W., 250 Camus, P., 246 Canul, R.. 186 Carey, S. N.. 153. 186 Caron, L., 32.48 Carothers, Z . B., 60,90,93 Carroll, S. M., 187 Casadevall, T. J.. 154, 191 Casagrande, P. J., 190 Cave, C. F., 62,89,92 Cawood, A. H., 93 Chaloner, W. G., 166, 176, 180, 186, 189 Chamisso. A., von, 55,93 Champagne-Philipe, M., 246 Chaney, R. W., 179, 186 Charlson, R. J., 242,243 Chiang, K. G., 83,93 Cho, S. H., 24, 27.48,49, 53 Choudhury, M. K., 49 Christiansen, R. L., 153, 186 Clark, D. K., 245 Clarkson, D. T., 38,40,49 Clayton, J. R., 244 Cleveland, J. S . , 244 Cleve, P. T., 196 Clift, R., 104, 186 Cochems, N., 49 Codispoti, 21 5 Coffin, 1 14, 118, 157

AUTHOR INDEX

255

DeMaggio. A. E., 84, 89 Cohen, A. D., 190 Colebrook. J. M., 198,210,227, 242, 243 Denman, A. W., 217,249 Coleman. J. M.. 143. 150, 186 Denman, K . L., 248 Colijn. F., 25 I Dessort, D., 48 Collinson, M. E., 117, 118, 124, 125, 186 Devol,A. H., 191,207,213,247 Collos, Y ., 207. 208. 243. 244, 250 Dickinson, H. G.. 67,68, 69, 82,85, 87, Conn, E. E.. 13,45, 53 88, 89.9 I , 92,93 Conway, D. V. P., 225,226,251 Dickson, R. R.. 194,232,238,243 Coombs, J. L.. 47.49 Diel, S . , 225, 226,244,245 Cooper, L. H . N.. 212,213,244.246 Diers, L., 60, 89 Digby, L., 71,90 Corner. E. D. S., 207.210.21 I . 244 Correns, C.. 85. 89 Dilcher, D. L., 104, 13I , 189 Correns. C. W., 177, 186 DiMichele, W. A,. 178, 189 Cottrell. J. C.. 25 I Dittus, W. P. J., 110, 186 COVC.D. J . . 90 Dixon, P. S.. 197. 248 Covington. D.. 143, 186 Dohler, G.. 20,49 Cowles. T., 244 Dokulil. M., 250 Crabbcndam. K. J . . 56.89 Dopp, W., 70, 7 I , 89 Craig, H .. 2 15. 244 Dorf, E., 151, 186 Craighead. F. C.. I 10. 186 Dortch, Q., 208, 244 Crcbcr, G. T., 166, 186 Doucc. R.. 13. 14. 34, 3 5 4 6 , 52 Crepet. N . L.. 130. 186 Doue, R., 50 Creutzbcrg. F.. 236,239.244 Douglas, D., 246 Cross. A. T.. 174, 186, 190 Douglas, D. P., 187 Cullen. J. J., 247 Douval. J. C.. 52 Cummins. K . W., 106, 123, 186, 189 Doyle, J., 65.69, 70,90,91 Cuneo, R.. 181, 186 Doyle. W . T., 90 Cunningham. C.. 246 Drebcs, G.. 197, 244 Curtis. P. J., 248 Dring, M. J.. 194, 204, 214,244, 246 Droop, M. R., 207,208,244,251 Cushing, D. H . . 196.216.225,235,244 Cutter, E. G., 90 Drum, R. W.. 177, 186 Dubaca, J. P., 48 Dubacq, J. B., 52 D Dacey, J . W. H., 240.244 Dubinsky, Z., 203, 204,244,245 Dagg. M., 21 I . 244 Duckett. J. G., 58, 59, 62, 89.90, 92 Ducklow, H . W., 212,244 Daghlian, C. P..130, 186 Daniel, J. Y.. 248 Duffield, W. A,, 160, 186 Dannell, G. S., 123, 186 Dugdale, R. C., 195,207,208,210, 213, Darley. W. M.. 49 244 Daro, M. H., 226,244,247 Dunstan, W. M., 206, 250 Datz. G.. 20,49 Dunwiddie, P. W., 108, 166, 173, 186, Davies, A. G., 207,210,21 I , 224, 244 187 Davies, C. L., 10, 51 Dupont, J., 243 Davies, J . M., 2 14,225,239,244 Dupouy, C., 246 Davis, P. G., 244 Durand, B., 145, 187 De Bock, P., 117, 187 Dzurisin, D., 166, 191 De Vries, H . , 123, 186 Deane, E. M., 50 E Ebel, F., 105, 187 Decadt, G., 243 Dedeurwaerder, H., 243 Edmonds, R. L., 108,187 Edwards, A., 202,251 Degges, C. W., 187 Dehairs, F., 243 Efremov, I . A., 97, 187 Delwiche, C. C., 252 Egan, B., 245

256

AUTHOR INDEX

Eggert, D. A., 177,188 Eggler, W. A,, 172, 187 Egglisher, H. J., 106, 187 Eglinton, G., 243, 250 Egmond, P., van, 92 Ehrensberger, R., 77,90 Eichenberger, W., 5,6, 10, 1 I , 13,22,33, 45,46,47,49, 5 I , 52 Eilertson, H. C., 234,244 Ekberg, I., 88 Elmore, H. W., 75,90 Elovson, J., 4, 10, 33,48,49 Elwood, J . W., 189 Eppley, R. W., 195, 197,202, 207, 208, 209,212,213,216,223,244,246 Erga, S. R., 234,244 Eriksson. G., 88 Erwin, J., 50 Esaias, W. E., 243,250 Estep, K . W., 197,244 Ettl, H., 70, 72, 80,90 Evans, J., 49 Evans, L. V., 73,90 Evans, R. H., 245 Evans, R. I . , 64, 89 Evans, R. W., 20,22,23,49 Evans, W. D., 178, 187 Eyme, J., 65,90 F Falkowski, P. G., 202, 204, 244,245, 246,250 Farmer, J. B., 71,90 Fasham, M. J. R., 200,202,204,2 17, 245 Fattom, A., 51 Fay, P., 50,90 Feige, G. B., 2, 13, 14,49 Feliciano, J. M., 178, 187 Fenchel, T., 243 Fergson, 117 Ferguson, D. K., 104, 105, 106, 107, 108, 109, 110, 112, 113, 117, 123, 124, 144, 171, 187 Ferguson, R. L., 207,245 Ferrari, R. A,, 45,48,49 Field, J. G., 243 Fisher, S. G., 113, 187 Fisk, L. H., 151, 187 Floodgate, G. D., 245 Flynn, K . J., 207,224,245 Fogg, G. E., 197,204,214,226,236,245 Foley, A. A.,7,49

Folkard, A. R.. 221,247 Forest, C. L., 58.90 Fork, D. C., 18.49 Forster, G. R., 249 Foster, P., 223,224, 235, 237, 245, 250 Fowke. L. C., 71,90 Foyn, B. R., 82.90 Francis, J . E., 166, 187 Franks, R., 84,90 Fransz, H. G., 225, 231,232. 233.238. 239,243,245 Fraser, C . J.. 185 Freeberg, J . A,, 76.90 Frentzen, M., 34.49 Fried, A., 22.49 Fritz, W. J., 157, 162, 163. 164. 165. 187. 188

Froggatt, P. C.. 155. 187 Frost, B. W., 210.21 I . 245,250 Frova, C.. 92 Fuhrman, J. A., 207.245 Furuya, M.. 5, 10, 22. 33. 52 G Gaarder, K . R., 197,246 Gabarajeva, N. I., 66.90 Gachter, R., 250 Gadow, H., 172, 187 Gagliano, S. M., 186 Gallagher, J. L., 145, 187 Gallegos. C. L., 249 Garrett, C., 248 Garside, C., 207. 213,245 Gastaldo, R. A., 103, 122. 128, 129. 133, 142, 144. 145, 146-147, 148, 180, 182, 187 Gastony, G . I., 81, 90 Gauzens, A. L., 250 Geider, R., 250 Geiger, N. S., 171, 188 Gerber, A., 1 I , 47,49 Gerlach, S. A., 223,245 Gieskes, W. W. C., 214, 225, 231,232, 234,238,239,245,251 Gifford, E. M. jr., 68,93 Gilbert, G. K . , 133, 187 Gilbert, P. M., 245,247 Gilbert, V. C., 110, 186 Ginzburg, B.-Z., 49 Ginzburg, M . , 49 Girty, G. H., 187 Given, P. H., 190 Gjems, O., 99, 186

AUTHOR INDEX

Glicken, H., 190 Goebel. K., 75. 90 Goering, J. J.. 195. 244 Gocyens, L., 243 Goldman. J. C.. 202, 207. 208. 209,2 12, 2 15.2 I6,243.245.246,247 Goodenough. U . W., 58.91 Goodsalk, G. L., 189 Gordon. H. R . . 216,245 Goreham. E.. 99, 186 Gosse, P.. 243 Gottesman, S., 80, 90 Could. H. R.. 142. 187 Gounaris. K., 2. 13. 32,45.49 Grace. J. R.. 186 Graham.A.. 151. 187 Graham. L. E.. 56. 57. 65. 90 Gran. H. H., 196 Grant. P.. 190 Gray. J . S.. 243 Greer.A.C.. 114. 117. 119. 120. 121. 125, 138, 190 Gregson. B. P., 191 Crier, C.. 108 Griffiths, D.. 245 Griffiths, D. K.. 219,220,249 Griffiths. G.. 28.49, 53 Grimley. N . H.. 80. 90 Groom, S., 220 Gros, P.. 232, 245 Grot, A. V., 49 Guest, K . P., 214, 246 Gulliksen, 0. M . . 90 Gurr, M . I., 44,45,46,49 Gusev, M . V.. 20,49

H Hafsaoui. M., 249 Hagberg, A.. 90 Hagberg, G., 90 Hague, A., 151, 187 Haines, T. H., 10,49 Hall, K . C., 49 Halpern, C. B., 172, 187 Hamazaki, Y., 51 Hanlon, R. D. G., 124, 188 Hann, A. C., 53 Hansen, V. Jr., 194, 250 Harbour, D. S.. 197, 198,235,236,243, 246,248 Hargraves, P. E., 244 Harmon, M. E., 172, 187 Harrap, R., 246

257

Harris, G . P., 196, 245 Harris. J. R . W.. 251 Harris, P., 49, 51 Harris, R. P., 224, 226, 245. 246 Harris, R. V., 42,43,44,49, 51 Harris, T. M.. 176, 188 Harrison, J. D., 51 Harrison, S., 163, 164, 187, 188 Harrison, W. G., 195. 196,204, 207. 209, 2 1 I , 2 13. 2 15, 230. 244, 245, 246, 249 Hartley, B.. 197, 246 Harvey. H. W., 196,212,246 Harwood. J. L., 3-53 passim Hasclkorn. R., 13. 50 Hassell, P. R., van, 53 Hauflcr, C. H.. 93 Haugen. E. M., 197,248 Hayward, T., 21 5,244 Head, P. C.. 246 Head. R . N.. 205,246,249 Heaney, S. I., 209, 246,25 I Heath. G. W., 131, 188 Heath, M . R.. 249 Hegeman. J., 232,243 Heilbronn. A,. 76, 90 Heimdal, B. R., 197, 209, 234, 243, 244. 246 Hein, E., 50 Heinemann, B., 249 Heinemam, K., 248 Heinemann, K . R.. 251 Heinen. W., 186 Heinroth, L., 226,247 Heinz, E., 34,48,49. 52. 53 Henderson, E. W., 199,250 Hendrix, L. B., 172, 188 Hepler, P. K., 63,91 Herbert, D., 247 Herd, Y. R., 66,90 Heslop Harrison, J., 67,68, 77, 82, 83, 89,90,91 Heymann, V., 244 Hickel, W., 242, 246 Hickey, L. J., 191 High, L. R., 131, 189 Hirsch, A. M., 75, 90 Hitchcock, C., 6, 14, 45, 50 Hitchcock, G . L., 214,246 Hobday, D. K., 150, 188 Hobson, L. A., 214,246 Hoffman, L. R., 58, 59,90 Hofmeister, W., 56, 90

258

AUTHOR INDEX

H~jerslev,N. K., 221, 223, 246 Holcomb, R. T., 191 Holligan, 197-249 passim Holm-Hansen, O., 49 Holton, R. W., 18, 50 Holt, V. I., 186 Holyoak, D. T., 143, 188 Holzer, G., 53 Homan, W. L., 92 Hopkins, A. W., 65,90 Horne, E. P. W., 247 Horner, H. T., jr., 65,68,90 Horvath, I., 53 Horwood, J. W., 201,217,234,246 Howard, F. O., 186 Howe, S., 244 Howland, R. J . M., 248 Howling, D., 42,44. 50 Hsia, Y., 191 Hulanicka, D., 12, 50 Hulbary, R. L., 65,90 Hummerstone, L. G., 40,48 Hunter, J. R., 150,242,218,250. 251 Hunt, H. G., 250 Hunt, J. W., 188 Hunt, R. J., 187 Hushovd, 0.T., 78.90 Hutchinson, D. E., 131, 188 Hyams, J. S., 92 Hynes,H. B. N., 105, 106, 122, 124, 188

I Ichimura, S., 247 Iddings, J. P., 187 Iijima, N., 50 Iler, R. K., 177. 188 Mias, Z. M., 77, 90 Ingram, L. O., 20, 51 Ito, S., 48 Itoh, S., 91 Izmailow, R., 72,90 J Jackson, G. A., 206,2 10,2 1 I , 246 Jacob, N. J., 248 Jacobson, D. M., 226,246 Jalouzot, M.-F., 70,90 James, A., 205,246 James, A. T., 26,43,45,48,49, 50, 51 Jamieson, G. R., 28,38,50 Janda, R. J., 161,188,191 Janero, D. R., 45,46,47, 50 Janzen, D. H., 105,188

Jaworski, J. G . , 17, 53 Jayasekera, R. D. E., 79.90 Jefferson, T. H.. 164, 165, 177, 188 Jelsema, C. L., 46, 50, 51 Jenkin, P. M., 2 13,246 Jenkins, W. J., 246 Jensen, K. G., 65.90 Jensen, W. A.. 64.69. 92.93 Jernik. J., 105, 188 Jewson, D. H., 194,203.204.214.244. 246 Jobson, S., 91 Johansen. K., 239.247 John, A. W. G., 249 Johnson, K. S., 215.246 Johnston, R., 223.246 Joint, I. R., 197. 198. 201.212.222. 226. 227.23 I , 232.234. 236. 237, 239. 247.25 1 Joiris, C:. 194. 212,214. 231, 239, 241, 247 Jones, A., 246 Jones, A. L., 3, 28, 30, 32. 33, 34, 35. 39, 40,41,42,50,51 Jones, D. A,, 245 Jones, K., 25 I Jones, K. J., 247 Jones, P. G. W., 223,246 Jones, R., 194, 236,239,247 Jopling, A. V., 133, 134, 188 Jordan, M . B.,227,234,236,237,247 Joyard, J., 13, 14, 34, 35.46, 50 Judkins, D., 244 Jupin, H., 48 Juszko, B. A.. 248 K Kahng, S. H., 214,250 Kames, W. H., 142,188 Kana, T. M., 204,247 Kapil, R. N., 64,69,90 Karowe,A. L., 164, 165, 177, 188 Kasha, K. J., 77,90 Kassab, J. Y., 245 Kates, M., 10, 1 I , 13, 20, 21,45,48,49, 50,52 Kaur, D., 63,90 Kaushik,N. K., 122, 123, 124, 188 Kawaguchi, A., 7, 10,35,48, 50 Kawalczewski, A., 124, 188 Kayama, M., 28,50 Kelley, B. C., 65,90 Kelly, W., 51

AUTHOR INDEX

Kenrick, J. B., 9, 50 Kenyon. C.N., 7, 14,20,50 Kermicle, J. L.. 77, 90 Khalanski, M., 243 Kidston, R., 151, 188 Kieffer, S. W., 153, 188 King, F. D., 202,207.208.210,213,247 Kiorboe, Th.. 239. 247 Kirk, T. 0..203.247 Kishino, M., 203, 247 Kleiffer, 153 Klein Breteler. W. C. M., 226,244 Kleppinger-Sparace, K. F., 13, 51 Klis, F. M.. 89, 92 Klug. M. J., 186 Knoll, A. H., 177, 188 Knowlton. F. H.. 187 Knox, R. B.. 77.91 Knox. S . , 243 Kojan. S., 93 Kok, A,, 25 I Konar, R. N.. 64.77.91 Koutsikopoulos, C.. 248 Kraay, G. W., 231,232.234.245 Krassilov, V. A , . 99, 188 Krespki, W. J.. 19, 50, 51 Kuiper, P. J. C., 53 Kuligowski-Andres. J., 93 Kumari, L.. 83,91 Kummel. F., 187 Kuparinen. J., 214. 247 Kuroiwa, T.. 91 Kwa, S. H., 75, 91

L La Rue, C. D.. 77.91 Laccadena, J.-R., 77.91 Laird, S., 71,91. 93 Lal, M., 59, 60, 73,75, 79, 81,91 Lambein, F., 9, 13, 50 Lampitt, R. S., 243 Lancelot, C., 226,232,239,247 Landriau, G . , Jr., 248 Lang, W. H., 75,91,I5l, 188 Lange, F. de, 75, 151,243 Larsen, D. W., 171, 188 Laur, M.-H., 2, 30, 52 Laurier, D., 185 Lavin-Peregrina, M. F., 249 Laws, E. A,, 208,209,247 Lawton, E., 75,91 Lazarenko, A. S., 73, 82,91 Lazaroff, N., 56,91

259

Le Caro, F., 1 13, 188 Le Corre, P., 248, 25 1 Le Coz, J. R., 248 Le Fevre, J., 219,237, 241, 247, 248 Lebour, M. V.. 197,246,247 Lee, A. J., 217, 221, 247 Lem, N. W., 16,17,50 Lemmon, B. E., 65,89 Lennon, H. J., 225,250 Leo, R. F., 177, 188 Lenten, N. R., 90 Lesnyak, E. N., 91 Levine. R. P., 45,48 Lewis, D.. 88, 89 Lewis, M. R., 194,207,246.247 Li, F. L., 67,91 Li, W. K. W.,209,216,247 Liddicoat, M., 243 Lien, S., 53 Lignell, A,, 40, 50 Likens, G. E., 113. 187,252 Lindahl, O., 226. 247 Linley. E. A. S., 226,246.248 Linscheid, M., 53 Lipman, P. W., 152, 188 Llewellyn, C. A., 197, 243,248 Lochte, K.. 226,245,247 Loder, J. W., 207.218,229,237,248 Loeuw, J. W. de, 243 Loh, C. S.,91 Lohmann, H., 196 Longman, K. A., 105, 188 Looby, W.J.. 69.91 Lorenzen, C. J., 197,2 1 I , 2 16,248,25 1 Lovelock, J. E., 240, 243, 248 Lucas, M. I.. 246 Luhr, J. F., 191 Lynch, D. V.. 22-24,25,26,50,51 M McBride, G. E., 65,90 McCabe, P. J., 148, 149, 150, 15 1, I88 McCarroll, S. M.. 187 McCarthy, D. G . ,245 McCarthy, J. J., 207, 248,250 McConchie. C. A., 63,91 MacGinitie, H. D., 132, 188 MacGregor, M., 122, 188 Mackas, D. L., 219,237,248 Mackenzie, A., 83,90 MacLeod, N. S., 191 Mcmanns, T. T., 52 McManus, J., 145, 188

260

AUTHOR INDEX

McQueen, D. R., 137, 188 Maddock, L., 201,227,232,242,248, 249 Mahlberg, P. C., 72, 77,9 I Mainx, F., 72. 91 Malej, A,, 224, 226, 245 Mamay, S. H., 177, 188 Manko, Yu. L., 172, 188 Mankura, T., 50 Manny, B. A,, 186 Manton, I.. 75. 81, 82,91 Mantoura, R. F. C., 197,243,248 Mantz, P. A,, 121, 188 Mardell, G. T. M.. 219,246,249 Margalef, R., 200. 240, 248 Marlow, I . T., 243 Marra, J., 204,248, 251 Marsden, C. R., 72,91 Marshall, S. M., 213,248 Martin-Jezequel, V., 222, 248, 249 Martin, N. C., 58,91 Martinson,. H . A,, 188 Mascarenhas, J . P., 78,84,90,93 Mathews. C . P., 124, 188 Mathot, S., 247 Megard, R. O., 194,215,248 Mehra, P. N., 75, 81, 83, 91,92 Mendiola-Morgenthaler, L., 47,51 Menon, M. K. C., 73,91 Mercer, E. I., 10, 13, 51 Meyer-Reil, L. A., 243 Miall, A . D., 126, 184, 188 Michaels, A. S., 46, 50, 51 Michel, H. P., 49 Millay, M. A., 177, 188 Miller, C. C. J., 90 Miller, J. A., 48 Mitchelson, E. G., 221, 248, 249 Miura, Y . ,52 Moal, J., 239,248 Mogensen, H . L., 63,91 Mohy-Ud-Dhin, M. T., 19, 51 Moitra, A., 64,67,91 Molder, M., 67,92 Mommaerts, J. P., 215. 220,243,247, 248 Moore, T. M., 13, 33, 51 Moorhouse, R., 45,51 Morel, A,, 203, 248 Morel, G., 75,91 Morgan, J. P., 142, 188 Morin, P., 224,248 Morley, R. J., 150, 189

Morris, I., 202, 240, 248 Morris, L. J., 43, 44, 50, 51 Morris, R. J., 250 Moshiri, G. A., 189 Mudd, J . B.. 13,45. 51, 52, 53 Mueller-Dombois, D.. 172. 190 Miiller, D. G., 81,90,91 Muller, J., 150. 186 Mullineaux, D. R., 152. 188 Murata, M..2,7,9, 13. 14, 15, 16. 17. 18, 19, 23. 34, 52 Murata. N., 48.49, 51. 52 Murphy, L. S., 197.248 Musgrave, A., 89.92 Myles, D. G.. 63, 79.91

Iv Nakamura, S.. 79.91 Nemoto, Y.. 52 Neumann, K.. 90 Nevissi, A. E.. 191 Newbold. J . D., 124. 189 Newell, R . C., 226. 246. 248 Nichols, B. W., 6, 10. 12, 14,44.45,48. 50, 5 1. 52 Nichols, J. H., 246 Nijs, J., 247 Nikitina, K . A,, 49 Nishida, I., 7, 9, 13, 14, 15, 19, 51 Nodby, O., 90 Nolan, K. M., 188 Norman. H. A., 5. 24,25. 26-27. 33.47, 51,53 Norstog, K.. 63. 77,91 Nusch, E. A,, 250 Nygren, A,, 72,91 Nykvist, N., 122, 189

0 Oakey, N. S., 247 Ohnishi, J., 35, 51 Okami, N., 247 Olesens, N. J. P., 247 Olson, G. J., 20, 51 Omata, T., 14,48,51 Onore, M., 50 Ooya, N., 76,91 Oren, 20 Orr, A. P., 213,248 Ostenfeld, C. H., 196 Ottaviano, E., 92 Otto, G. H., 100, 189 Oudin, J. L., 187

26 1

AUTHOR INDEX

Overton, E., 56,92 Overton, J. B., 73, 92 Owens, J. N.. 67,92 Owens, N. J. P., 228,243,247,248 Ozaki. K.. 126, 189 Ozer. J., 248

P Paasche, E., 209,248 Padan. E.. 51 Paerl. H. W.. 205,248 Palta, H. K.. 75. 92 Pang, Y. H., 121, 189 Paolillo. D. J., jr., 65, 92 Parke. M.. 197,248 Parker. W. C.. 189 Parrish. J. T.. 105. 124, 129. 176, 182, 183, 189. 190 Parry. D.. 92 Parson. M . J.. 92 Parsons. T. R.. 197.25 1 Partensky. F.. 236.248 Pashuk. C . T..91 Paync. R. E., 220. 225.239.244.248 Peavey. D. G.. 245 Pederson. M., 50 Pederson. S. M.. 249 Peebles. M . W., 187 Peel. M. C., 58.92 Pennell, R. I., 62,63,64,67. 69, 78,85, 87.89.92 Pennycuick, L., 219. 233, 234, 249 Peppers, R. A., 189 Pcsch, R.. 53 Petersen, R. C., 123, 186, I89 Peterson, B. J., 207, 212, 213, 214, 223, 244,248 Peterson, D. W.. 153, 186 Pettitt, J. M., 66, 68, 87, 88, 92 Pettitt, T. P., 50 Pettitt, T. R., 2, 3, 7, I I , 12, 30.31, 32, 35, 37,51 Petzold, T. J., 203,243 Pfefferkorn, H. W., 112, 143, 146, 183, 190, 191 Pflaumann, U., 243 Pham-Quang, L., 2,30,52 Philipson, M., 86,92 Phillips, T. L., 177, 178, 189 Phinney, D. A., 250 Picard, M. D., 131, 189 Pichot, G., 248 Pickett-Heaps, J. D., 58, 59, 71,90,92

Pickmere, S. E., 78,92 Pierson, T. C., 161, 189, 191 Pingree, R. D., 196-249 passim Piorreck, M., 20, 52 Pipe, R. K., 197,201, 247 Platt, T., 195, 196,202,204,209,213, 2 15,2 17, 2 18,227, 229, 230,237, 245,246,247,248,249,250 Plumley, F. G., 145, 187 Pobiner, 89 Pohl, P., 5,6, 12, 28, 38, 52 Pohlheim, F., 86,92 Polack, W., 150, 189 Pomroy, A. J., 198, 2 12,222, 23 I , 232, 234,239,247,248 Pond, V., 93 Ponzelar, E., 49 Porter, E. K., 67,92 Postma, H., 222,223,224,232,242,249 Potonie, H., 112, 189 Potter, F. W.. 130, 189 Potter, U., 67,69,85, 89 Poulet, S. A., 224,249,252 Praeger, R., 1 17, 189 Preisendorfer. R. W., 203,249 Prestegaard. K. L., 191 Pringsheim, N., 73,92 Pugh. P. R., 245,246.249 Purdie, D. A,, 244,246, 251 Pytkowicz, R. M., 246

Q Quatrano, R. S.. 89 Queguiner, B., 224,249

R Radach, G., 196, 198, 199,217,227,242. 246,249 Radunz, A,, 53 Raghaven, V., 84,92 Rai, H., 250 Raine, R. C. T., 215,249, 251 Ramsay, H. P., 65,92 Rau,G. H., 108, 109, 123, 132,189 Raven, J. A., 194,204,249 Raymond, A., 143, 184,186,189 Rebeille, F., 40, 52 Redfield, A. C., 206,212,249 Rees, E. 1. S., 245 Reid, E. H.,28, 38, 50 Reid, J. L., 21 5,250 Reid, P. C., 198, 199, 232,235, 242,249

AUTHOR INDEX

262

Reiners, W. A,, 252 Rember, W. C., 132, 151, 190 Remy, R., 7, 52 Renger, E. H., 244 Retallack, B., 59,92 Retallack, G. J., 178, 189 Rex,G. M., 121,122, 176, 177, 178,179, 180, 189, 190 Rhamstine, E., 77,91 Rhodes, E. G . , 145,189 Rice, A. L., 243 Rich, F. J., 132, 189 Richards, P. W., 113, 189 Richardson, K., 204,206,214,235,236, 237,249 Richardson, P. J., 108, 189 Rick, C. M., 93 Ridley, H. N., 117, 189 Rietema, H., 70.92 Rijpstra, W. I. C., 243 Riley, G. A., 21 3, 250 Riley, J. P., 243 Ripetsky, R.T., 75,92 Rippka, R., 50 Risk, M. J., 145, 189 Robert, D., 64, 92 Roberts, J. K. M., 49 Robinson, G . A., 198,242,250 Robinson, H. P., 49 Rodkiewicz, B., 69,85,92 Roessler, P. G., 47, 52 Rolfe, W. D. I., 189 Roman, M. R., 21 1,250 Romanov, V. V., 150, 189 Roomans, G. M., 50 Roth, J. L., 104, 131, 189 Rothwell, G . W., 177, 189 Roughan, G., 32,34,52 Roughan, P. G., 31,52 Rowe, G. T., 239,250 Rowlands, C., 49 Rudd, R. L., 113,188 Rullkotter, J., 34, 52 Runnegar, B., 100, 190 Russell, F. S., 234,238,246 Russell, N. J., 3, 50 Russell, S. D., 63,92 Ryckaert, M., 232,245 Ryther, J. H., 206,216,250 S

Sado, T., 50 Safford, R., 45,52

Sager, G., 218,250 Sager, R., 79,92 Saint John, H., 173, 190 Sakamoto, M., 214,250 Sakurai, T., 48, 50 Samain, J. F., 248 Sammler, R., 218,250 Samson, M. R., 56,92 Sangwan, R. S., 67,92 Sari-Gorla, M.. 78,92 Sarnthein, M., 243 Sastry, P. S., 45, 52 Sato, N., 2, 5.7, 10, 1 I , 14. 15, 16, 17. 18, 19,22,23,33,34,35,49, 51, 52 Savidge, G . ,204, 225,235, 237, 245,250 Schanze, F., 244 Schedlbauer, M. D., 78.92 Scheihing, M. H., 110. 143, 146. 190 Schiller, J., 197, 250 Schlapfer, P., 13.46, 52 Schnitzer, M. B., 243 Schoklitsch, A., 121. 190 Schopf, J. M., 175, 177, 190 Schopf, J. W., 100, 190 Schraudolf, H., 66,92 Schulenberger, E., 215,250 Schulz, P., 69.92 Schulze, M. S., 189 Schumm, S. A., 126,190 Scott, A. C., 148,177, 178, 190 Scott, J., 59, 89 Scott, K. M., 188 Scrope-Howe, S., 245 Sedell, J. R., 191 Sequin-Swartz, G . ,77,90 Seyama, Y., 52 Sharp, J. H., 244 Shaw, W. R., 77,92 Sheffield, E., 59,66,67,71,75,76,79,83, 93 Sherman, L. A., 18,52 Shields, A., 121, 190 Shim, J. H., 214,250 Shimakata, T., 41, 52 Shimizu, Y., 243 Sieburth, J. McN., 244 Siersma, P. W., 83,93 Sigee, D. C., 63,79,93 Sigleo, A. C., 177, 190 Sigurdsson, H., 153, 160, 167, 186, 190 Simpson, J. H., 218,219,248,249,250 Simpson, J. J., 251 Sinclair, M., 239,250

263

AUTHOR INDEX

Singh, M . N., 77.91 Slack, C. R.. 52 Slack, R.. 34, 52 Slawyk, G., 207,244 Sleep, J. A., 224,244 Smathers, G. A., 172, 190 Smayda, T. J., 200,250 Smiley. C. J.. 132, 151, 190 Smith, D. G., 126, 171. 190 Smith, D. J., 240, 250 Smith. K . L., 3.6. 7, 10. 24. 30, 31, 32, 35, 37.40.41, 52, 53

Smith, L. A.. 51 Smith. R. C.. 217. 250 Smith. R. E. H., 214,250 Smith, S., 244, 250 Smith, W. G . . 186 Smithers, J.. 249 Sossountzov. L.. 93 Sournia, A,. 236,248 Southward, A. J., 242.250 Spackman. W., 149,190 Sparrow. A. H.. 67,93 Spicer, R. A.. 99-190passim Stahl. E., 73.93 Stanier, R. Y., 50 Stanton. T. W., 187 Stapleton, S. R.. 17, 53 Starkey, R. L., 186 Stark. R. W., 189 Steele, J. H.,196, I99,2 10,2 12,229, 231,233. 234, 235,238,241, 242, 250 Steeman Nielsen, E., 194,214,250 Steeves, T.A., 75,93 Steil, W. N., 75, 93 Stettler. R. F., 93 Stewart, E., 244 Stewart, K. D., 68,93 Stobat, A. K., 49 Stobbart, K., 53 Stopes, M. C., 177, 190 Stosch, H. A., von, 90 Strasburger, E., 56,93 Strathman, R. R., 197,250 Strickland, J. D. H., 197,251 Stumpf, P. K., 13, 16, 17,41,45, 50, 52, 53 Sturm, B., 203,221,223,251 Styan, W. B., 143, 145, 146, 190 Stymne, S., 49, 53 Suberkropp, K. F., 186 Suire, C., 65,90

Sulkyan, D. S., 81,91 Sverdrup, H. 0.. 194,251 Szczepanski, A., 108, 190

T Taggart, R. E., 174,186, 190 Takahashi, M., 247 Takahshi, N., 51 Takemaro, S., 48 Talling, J. F., 196,246,251 Tanksley, S. T., 78,93 Tanner, C. E., 78,8 1,93 Tasen, J. P., 234,244 Taylor, A. H., 223,227,230,242,243, 25 1

Taylor, C., 65,90 Taylor, T. N., 177, 191 Teichmuller, M., 147, 149, 150, 191 Teichmuller, R., 147, 149, 150, 191 Tett, P., 202. 209.2 12,2 I6,2 17,230, 236,237.25 1

Thingstad, F., 243 Thomas, B. A., 99, 142, 190 Thomas, G.. 51 Thompson, G. A., 5,22-24,25,2627, 33,47,48,49, 50, 51, 53 Thoresen, S. S., 244 Thouvein, J., 185 Throndsen, J., 197, 251 Tietz, A., 49, 51 Tijssen, S. B., 221,25 1 Tilling, R. I., 186 Tilzer, M. M., 246,250 Topliss, B. J., 203,221,251 Tornabene, T. G., 6,47,48,53 Tourte, Y., 62.64,93 Tranter. P. R. G., 246 Tregner, P., 249 Tremblay, H. J., 239,250 Tremblay, P., 48, 50 Tremolieres, A., 52 Trew, D. O., 25 1 Tryon, A. F., 66, 93 Tschumi, P., 250 Tulecke, W., 77,93 Tulloch, A. P., 48, 52 Turley, C. M., 207,224,226,245,247, 25 1

Turner, F. R., 58,93

U Ueta, N., 52 Uncles, R. J., 231,251

264

AUTHOR INDEX

Ungerer, P. H., 187 Ursin, E., 194, 251

V Vagelos, P. R., 49 Van den Ende, H., 89,92 Varekamp, J. C., 160, 191 Vasil, I. K., 67, 88 Vaughan, P. W., 248 Vehlinger, V., 250 Veldhuis, M. J. W., 224, 230,232,251 Venekamp, L. A. H., 226,243,251 Verhagen, J. H. G . ,233,245 Vidal, J., 21 I , 246,251 Videau, C., 236,237,25 1 Vigh, L., 38, 53 Violette, D. L., 187 Viollier, M., 203,221,223, 246,25 1 Vishniac, W., 56,91 Voight, B., 191 Volcani, B. E., 48,49,50 Voltolina, D., 245 Vondy, K . P., 92 Vshivtsev, V. S., 49 Vucetic, T., 216,244

W Waaland, 72 Wafar, M . J. M., 225,231,233, 251 Wagner, V. T., 63,9 I , 93 Waide, J. B., 123, 124, 191 Waitt, R. B., 162, 166, 191 Wakeham, S. G.,240,244 Walcott, C. G . , 187 Walker, G . P. I., 187 Walker, K . A., 53 Walker, S., 75, 81, 82,91 Walker, T. A., 203,251 Walker, T. G . ,71,93 Walsby, A. E., 48 Walsh, J. J., 209,251 Walther, H., 187 Walton, J., 122, 176, 179, 180, 188, 191 Walton,T. J., 17, 19,48, 50, 51 Wandschneider, K., 201,251 Ward, B. B., 21 1,251 Warmke, H. E., 72,93 Warner, S., 177, 189 Warren, S. G . ,243 Watanabe, I., 90 Watson, D. M.S., 177, 190

Watts, J. L., 247 Weber, M. E.. 186 Weber, W., 90 Webster, J. R., 123, 124, 191 Weed, W. H., 187 Weekley, C. M., 246 Weering, T. C . E., van, 239,251 Wee, Y. C., 91 Wegner, G . ,223,232,243 Weichart, G . ,2 15, 234, 235, 25 I Welschmeyer, N. A., 21 I . 251 Welti, D., 48 Wetherbee, R., 89 Wettstein, F. von, 8 I , 93 Wetzel, R. G . , 186 Wharfe. J.. 31.48 Wheaton, J . E. G . . 245 White, 171 Whitfield, M., 194. 251 Whitledge. T.. 21 1.244, 250,251 Whittaker. R. H., 252 Whittier, D. P., 71, 75, 76. 90, 93 Wilde. P. A. W. J. De, 239, 25 I Wilkerson, F. P.. 207,213,244 Wilkinson, H. P., 178, 191 Williams, A. M.. 122, 191 Williams, P. J. Le B., 194,21 I , 213, 214, 243,244,246,251 Williams. P. M., 206,246 Williams, R., 224,225, 226, 247,251, 252 Willing, R. P., 78.93 Wilson, C. J. N., 187 Wing, S. L., 129, 131, 191 Winner, W. E., 154, 191 Winton, L. L., 93 Wiser, R., 48 Wissmar, R. C., 171, 191 Wnuk, C., 112, 191 Wolf, P. G . , 82, 93 Wolfe, J. A., 114, 120, 125, 133, 135, 138, 139, 140, 160, 174, 191 Wolk, C. P., 9, 13, 50 Wong, C. S., 246 Wood, B. J., 251 Wood, G . W., 49 Woodcock, C. L. F., 64,69,93 Woodward, E. M. S., 248 Woodwell, G . M., 194,252 Wrage, K., 49 Wright, D. G., 248 Wroblewski, J. S., 217,252 Wuycheck, J. C., 186 Wyman, K., 245

AUTHOR INDEX

Y Yamada, M., 35,48,51 Yamada, Y.. 50 Yang, H.-Y., 77,93 Yentsch, C. S., 216, 250 Yochelson, E. L., 177, 188 Yonge, C . H., 123, 191 Yoshioka, M., 243 You, R., 64.93 Yung. K. H.. 45.53 Yuretich. R. F.. 131, 191

Z Zamir, D., 93 Zbaren, D., 250 Zepke, H . D., 14,34,53 Zhou, C., 71,93 Zinsmeister, D. D., 60,93 Zurheide, F.. 5, 6, 12, 28. 38, 52

265

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SUBJECT INDEX

A Algae gametogenesis, 57-59 isogamous forms, 57-58 oogamous forms, 58-59 gametophyte/sporophyte shift, female gamete in, 78-80 life cycles, aberrant, 5 6 5 7 induced, 72-73 natural. 70 sporogenesis, 65 see also Lipid metabolism in algae; Phytoplankton, North-West Europe shelf seas Alternation of generations, 55-93 aberrant cycles, 70-77 induced, 72-77 natural, 70-72 causal approach to, 78-87 assumptions, 78 gametogenesis, 57-64 algae, 57-59 bryophytes/homosporous pteridophytes, 59-63 heterosporous pteridophytes/seed plants, 63-64 gametophyte/sporophyte shift, lower plants apogamy in, 80-82 female gamete in, 78-80 life cycles, universality of, 5 6 5 7 sporogenesis, 65-70 algae, 65 bryophytes, 65 heterosporous pteridophytes/seed plants, 66-70 homosporous pteridophytes, 65-66 sporophyte/gametophyteshift, 82-87 and apospory in lower plants, 83-84 megasporogenesis, 8 4 8 7 phase change and meiosis, 82-83 sporogenesis theory, 84

Apogamous cycles, homosporous pteridophytes, 70-71 APogamY in gametophyte/sporophyte shift, lower plant, 80-82 induced, and chromosome number, 82 natural cycles, 81-82 parthenogenesis, 80-8 1 induced, in pteridophytes heterosporous, 77 homosporous, 75 Apospory induced in ferns, 75 in flowering plants, 77 and sporophyte/gametophyte shift, lower plant, 82-84 Archegoniates gametophyte/sporophyte shift, female gamete in, 79-80 parthenogenesis, 81 Azolla, microsporogenesis, 66 B Bacteria and phytoplankton grazing, 226 Beaches, plant debris deposition on, 144-145 Bryophytes gametogenesis, 59-63 oogenesis, 59-63 spermatogenesis, 59 life cycles, aberrant induced, 73-75 natural, 70 sporogenesis, 65 sporophyte/gametophyte shift, and apospory, 82-83 C

Carbon fluxes and phytoplankton productivity, 21 3-21 5,230, 234

267

268

SUBJECT INDEX

Cell quota model for phytoplankton growth, 207-208 Channel deposits abandoned channels, 130 crevasse splays, 129 Carboniferous, plant community reconstruction, 180-181 fluvio-marine interdistributory embayments, 144 floodplains, 129-1 30 lag deposits, 126-127 levees, 128 point bars, 127 Charcoalification, 176 Cfdamydomonas gametogenesis, 58 life cycle, 56-57 lipid metabolism, 4 5 4 7 Chlorella spp. lipid metabolism, 4 2 4 5 Chlorophyta life cycles, 57 parthenogenesis in, 80-8 I Chlorosulpholipids, 3 4 Chromosomes in lower plants, apogamy and, 82 Coal autochthonous formation coalification, 148 environmental conditions, 148 floating mire development, 149 quaking bogs, 149 raised mire development, 149-15 1 carbonate nodules, 177-1 78 see also Charcoalification; Peats Coal balls, 177-1 78 Conifers, see Gymnosperms see also Trees, whole, fossil record Continuous Plankton Recorder (CPR), I98 Copepods grazing phytoplankton, 226 Crevasse splay deposits, 129 Carboniferous, plant community reconstruction, 180-181 fluvio-marine interdistributory embayments, 144 Cyano bacteria fatty acid composition, 7, 9 glycolipids in, 9 lipid metabolism, 13-19 fatty acid synthesis, 15-17 fatty acyl composition, 14 membrane composition, 13 and temperature, 17-19

Cyanophyta, life cycle, 56 D Deltas fluvio-lacustrine, 133-140 formation model, 133-135 Gilbert-type profile, 133 high-energy systems, 138-140 low-energy system, 135-1 38 in volcanic terrain lateral lakes. 170-171 fluvio-marine, 140-147 beaches, 144-145 distributory mouth bars, 142 interdistributory embayments, 144 lower plain marshes, 145-146 pro-delta slope, 141-142 tidal flats, 143-144 upper plain marshes. 146- I47 Detritivores phytoplankton consumption, 210 and plant fossil record, 105-106 Diaspores, aquatic mechanical degradation, 124-125 Dogger Bank phytoplankton productivity, 232 Dryopteris, natural aberrant cycles, 71 Dunaliella lipid metabolism galactosylation, 27 halotolerance, 20,22 labelling studies, 2 4 2 6 microsomal phospholipid retailoring, 26-27 and temperature, 22-24 Duripartic preservation, 176 E El Chichon (Mexico) 1982 eruptions taphonomic considerations, 159-160 lateral lakes, 170-1 71 vegetation preservation in tephra, 167-168 vegetation recovery, 174-1 75 F Fatty acids in algae, 5-9 marine, 28, 3 4 3 5 in cyanobacteria, 7,9 synthesis, 15-17 in Dunaliella spp., 22 metabolism, 12

SUBJECT INDEX

269

Ferns casts/moulds, 178-1 79 sporophyte/gametophyte shift compression/impressions, 1 75-1 76 apogamous cycles and, 8 1-82 duripartic preservation, 176 and apospory, 82-83 mineralization, 1 7 6 178 see also Pteridophytes quality of record, 98-100 Floodplain deposits, 129-1 30 assemblages, 99-100 Flowering plants, see Seed plants and deposition, 99 Fluorometry for phytoplankton and organ isolation, 99 productivity, 197-1 98, 21 6 2 1 7 and time-averaging, 98-99 Fossil assemblage formation/ sedimentary, 101,103-104 interpretation, 95-1 91 allochthonous/autochthonous aquatic processing, I 14-125 assemblages, 101, 103 floating, 115-1 19 settling velocity, 103-1 04 leaf degradation, 122-1 24 taphonomy, 98,179-183 community reconstruction, 180-1 81 water column transport, 119-122 dispersal by wind, 1061 12 community-suite/regional air fall, 108-109 reconstruction, 18 1-1 83 fall velocity. 106108 defined, 97 fossils in sedimentology, I83 post-descent, 109-1 10 storm effects, 1 1 0 - 1 I2 morphology and taxonomy, 180 fluvial transport. 125-130 potential of, 184-185 channel deposits, 126-1 30 trees, whole, preservation of, 114 fluvio-marine deltas/estuaries, 140vulcanism, 151-175 147 debris flow, 160-1 66 beaches, 144-145 explosive, case studies, 152-1 60 deltaic environments and lateral lakes, 168-1 71 assemblage composition, 147 and magma viscosity, 151-152 distributory mouth bars, 142 tephra, preservation in, 166168 interdistributory embayments, 144 vegetation recovery, 172-1 75 marshes, lower plain, 145-146 Frdzier River upper delta, 146 marshes, upper plain, 146-147 peats, detrital, 147 pro-delta slopes, 141-142 G tidal flats, 143-144 Galactosylation in Dunaliella lipid forest floor litter degradation, 112-1 14 metabolism, 27 heterogeneity, 100-101, 102 Gamete, female, and alternation of assemblage complexity, 10 I , 102 generations, 78-80 stability, evolutionary/spatial, 100 Gametogenesis, 57-64 integrated approach, 97,98 algae, 57-59 lacustrine environments, 130-140 isogamous forms, 57-58 fluvio-lacustrine deltas, 133-140 oogamous forms, 58-59 isolated lakes, 132 bryophytes/homosporous montane lakes, I3 1-1 32 pteridophytes, 59-63 ox-bow lakes, 133 oogenesis, 59-63 plant representation, 131 spermatogenesis, 59 leaf abscission, 104-1 06 heterosporous pteridophytes/seed peat/coal assemblages, 147-1 5 1 plants, 63-64 coalification, 148 Glossopterid fructifications, environmental conditions, 148 Carboniferous, 180 floating mire development, 149 Glycolipids, 2 quaking bogs, 149 in cyanobacteria, 9 raised mire development, 149-1 5 1 Granal stacking, and trans-A3preservation/diagenesis, 175-1 79 hexadecanoate, 7

270

SUBJECT INDEX

Gymnosperms megasporogenesis, 68-69 microsporogenesis, 6&67 oogenesis, 64 spermatogenesis, 63 Gyrodinium aureolum productivity in frontal regions, 236237

H Halotolerance in Dunaliella spp. and lipid metabolism, 20,22 Heavy metals, and lipid metabolism in algae, 40-42

I Irradiance and phytoplankton photosynthesis, 203

L Lacustrine environments and fossil record, 130-140 fluvio-lacustrine deltas, 133-140 formation model, 133-1 35 Gilbert-type profile, 133 high-energy systems, 138-140 low-energy systems, 135-138 isolated lakes, 132 montane lakes, 131-132 ox-bow lakes, 133 plant representation, 131 Lag deposits, 126-127 Lakes, lateral, in volcanic terrains, 168171 see also Lacustrine environments and fossil record Leaves abscission, 104-1 06 degradation, aquatic, 122-125 biological, 122-124 mechanical, 124 delta deposition, 135-1 38 and plant origins, 136.138 dispersal by wind and fossil record air fall, 108-109 post-descent, 109-1 10 storm effects, 110-1 12 floating, 1 15-1 17 fluvial transport, 125-1 26 settling velocity calculation, 103-104

factors in, 106-108 and water transport, 1 19-120 Lepidodendrids, Carboniferous, morphology, 180 Levees, 128 Life cycles aberrant, 70-77 algae, 70 induced, 72-77 natural, 70-72 universality of, 5 6 5 7 Light and lipid metabolism in algae, 35-36. 37 and phytoplankton growth, 202-204 North West Europe shelf seas, 220223 nutrient interaction, 208-209 see also Photosynthesis Lilium, microsporogenesis. 67-68 Lipid metabolism in algae, 1-53 Chlamydomonas reinhardtii, 45-47 Chlorella spp., 42-45 complex lipids, I3 composition in algae, 5-12 classes, 9-12 fatty acids, 5-9 cyanobacteria, 13-19 fatty acid synthesis, 15-1 7 fatty acyl composition, 14 membrane composition, I3 and temperature, 17-1 9 Dunaliella spp. galactosylation, 27 halotolerance, 20.22 labelling studies, 24-26 microsomal phospholipid retailoring, 2 6 2 7 phospholipids and temperature, 2224 fatty acid metabolism, 12 lipid structures, 2-5 marine, 28-42 fatty acid positions, 33-35 and heavy metals, 40-42 labelling chacteristics, 28-33 and light, 35-36,37 and temperature, 36,3840 see also Algae; Phytoplankton, NorthWest Europe shelf seas Litter degradation, and fossil record, 112-1 14 Liverworts, induced aberrant cycles, 75

27 1

SUBJECT INDEX

M Mangrove, 143 Marshes, delta plain lower, 145-146 upper, 146-147 see also Mires; Quaking bogs Megasporogenesis gymnosperms, 68-69 seed plants, 69-70 and sporophyte/gametophyte shift causal aspects, 85-87 features of, 84-85 Metals, see Heavy metals, and lipid metabolism in algae Michaelis-Menten relation and phytoplankton nutrient uptake, 208 Microheterotrophic organisms grazing phytoplankton, 226 plant carbon utilization, 21 1-212 Microsporogenesis pteridophytes, 66-67 see plants, 67-68 Mineralization of tissue, 176-1 78 Mires floating, 149 raised, 149-151 see also Marshes; Quaking bogs Mobile Delta (Alabama), 146 Monod equation, 207 Montane lakes, and fossil record, 131132 Mount Saint Helens 1980 eruptions, 152-158 blast effects, 153-1 58 debris flow, 160-1 63, 164-1 65 lakes, effects on, 171 mechanism, 152-1 53 vegetation recovery, 172-174 N Nevado del Ruiz eruption 1985, 165 Nitrate fluxes and phytoplankton production, 235 Nitrogen deficiency in algae, and lipid metabolism, 47 North West Europe shelf sea availability, 223-224 for phytoplankton, 206-207 excretion and grazing rate, 21 1 nutrient budgets, 212-213 Nostoc, life cycle, 56

Nutrients for phytoplankton, 204-209 growth models, 207 light interaction, 208-209 nitrogen, 206-207 limitation, 206 North West Europe shelf sea availability, 223-225 nutrient budgets, 212-213 and productivity estimates, 228-230 sources, 205 steady state conditions, 208

0 Oedogonium gametogenesis, 58-59 Oogenesis bryoph ytes/homosporous pteridophytes, 59-63 heterosporous pteridophytes/seed plants, 63-64 Ox-bow lakes formation, 130 plant deposition, 133 Oxygen fluxes and phytoplankton productivity, 213,214-215

P Parthenogenesis, and gametophyte/ sporophyte shift, 80-8 1 Peats autochthonous formation, 147-1 51 environmental conditions, 148 floating mire development, 149 quaking bogs, 149 raised mire development, 149-1 51 carbonate nodule formation, 177-178 deltaic, detrital, 147 lower marshes, 145-146 upper marshes, 146 mangrove, 143 see also Coal Permineralization, 177 Phaeophyta, life cycles, 57 Phospholipids, 2 Phosphate shelf sea distributions, 233234 Phosphorus North West Europe shelf sea availability, 223-224 as phytoplankton nutrient, 206 nutrient budgets, 212

272

SUBJECT INDEX

Photosynthesis by phytoplankton, 202204 carbon fixation, and productivity estimates, 230 estimation, and oxygen/carbon fluxes, 2 13-21 5 in frontal regions, 237 light availability, North West Europe, 22s223 see also Light Phytoplankton, North-West Europe shelf seas, 193-252 control of production, 202-212,241 grazing, 209-2 12 light, 202-204 nutrients, 202,204-209 temperature, 209 distributions, 196-202 descriptive accounts, 196-197 quantitative methods, 197-1 98 temporal/spatial, 198-202 variability, 241-242 environmental conditions, NW Europe, 2 17-227 annual production cycle, 226-227 grazing, 225-226 light availability, 220-223 mixing processes/seasonal stratification, 217-221 nutrient availability, 223-225 evaluation of productivity estimates, 227-238 carbon fixation, 230 frontal regions, 235-237 mixed waters, 231-233 nutrient budgets, 228-230 spatial/temporal variations, 237238 stratified waters, 233-235 plant material fate, 238-240 biogeochemistry, 239-240 sedimentation, 239 productivity estimation, 194-196, 2 12-21 7 biomass distributions, 215-217 future approaches, 242 lack of advance, 241 models, 217 nutrient budgets, 212-213 oxygen/carbon fluxes, 213-221 problems, 194 see also Algae; Lipid metabolism in algae

Pigment determinations of phytoplankton, 197-1 98 Plasma membranes, cyanobacteria, lipid composition, 13 Platyzoma, sporogenesis, 66 Point bars, 127 Pollution, see Heavy metals, and lipid metabolism in algae Polysiphonia, gametogenesis, 59 Psilotum, sporogenesis, 66 Pteridophytes heterosporous aberrant cycles, induced, 76-77 aberrant cycles, natural, 71-72 gametogensis. 6 3 4 4 magasporogenesis, 68-69 microsporogenesis, 66-67 homosporous aberrant cycles, induced, 75-76 aberrant cycles, natural, 70-71 gametogenesis, 59-63 sporogenesis, 65-66 see also Ferns Pyritization, 178

Q

Quaking bogs, 149 see also Marshes; Mires

R Redfield ratios, 206,2 12 Respiration by phytoplankton, 204 and carbon fixation estimates, 230 Rhodophyta, life cycles, 57 aberrant, induced, 72-73 Rivers aquatic processing of plant debris, 114-125 floating, 115-1 19 leaf degradation, 122-1 24 water column transport, 119-122 channel deposits, 126-130 abandoned channels, 130 crevasse splays, 129 floodplains, 129-1 30 lag deposits, 126-127 levees, 128 point bars, 127 nutrient discharge, 242 and phytoplankton productivity, 232-233 transport of plant debris, 125-126 see also Deltas

SUBJECT INDEX

S SU~PU, 55-56

Scalar irradiance and phytoplankton photosynthesis, 203 Sea, see Phytoplankton, North-West Europe shelf seas Season, and lipid metabolism in algae, 38,39 Secchi disc, 221 Sedimentation of plant debris from water flow, 121-122 Seed plants aberrant cycles induced, 77 natural, 72 gametogenesis, 63-64 megasporogenesis, 69-70 microsporogenesis, 67-68 Seeds, floating times, I 17-1 I8 SelugineIIu. megasporogenesis, 68 Settling velocity of plant debris calculation, 103-104 factors in, 106-1 08 in water, 119-120 Silicon deficiency in algae and lipid metabolism, 47 Silification, I77 Spermatogenesis bryophytes, 59 heterosporous pteridophytes/seed plants, 63 Sporogenesis, 65-70 algae, 65 bryophytes, 65 pteridophytes, heterosporous megasporogenesis, 68-69 microsporogenesis, 66-67 pteridophytes, homosporous, 65-66 seed plants megasporogenesis, 69-70 microsporogenesis, 67-68 and sporophyte/gametophyte shift, 84 Storms and plant dispersal, and fossil record, 1 1 0 - 1 12 Sulphur containing lipids, 3 T Taphonomy and fossil record, 98, 179183, 184-185

273

community reconstruction, 180-1 8 1 community-sui te/regional reconstruction, 181-183 defined, 97 fossils in sedimentology, 183 morphology and taxonomy, 180 Temperature and lipid metabolism in algae, 36, 3 8 4 0 in cyanobacteria, 17-1 9 in Dunaliellu spp., 22-24 and phytoplankton growth, 209 Tephra, vegetation preservation in, 166168 Thylakoid membranes, cyanobacteria, lipid composition, 13 Tidal flats, plant debris deposition, 143I44 Trees, whole, fossil record, 114 Trinity Lake (California) delta deposition, 138-140

V Vulcanism and plant fossil record, 151I75 debris flow, 160-1 66 El Chichon, 163-164 Mount Saint Helens, 160-163, 164165 Nevado del Ruiz 1985, 165 explosive, case studies, 152-1 60 El Chichon, 159-160 Mount Saint Helens, 152-1 58 lateral lakes, 168-171 and magma viscosity, 151-152 tephra, preservation in, 166-168 vegetation recovery, 172-1 75 El Chichon, 174-175 Mount Saint Helens, 172-174

W Wind dispersal of plant organs, 106-1 12 air fall, 108-109 fall velocity, 106-108 post-descent, 109-1 10 storm effects, I I s 1 12

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