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Ecology of Phytoplankton

Phytoplankton communities dominate the pelagicecosystems that cover 70% of the worlds surfacearea. In this marvellous new book Colin Reynoldsdeals with the adaptations, physiology and popula-tion dynamics of the phytoplankton communitiesof lakes and rivers, of seas and the great oceans.The book will serve both as a text and a majorwork of reference, providing basic information oncomposition, morphology and physiology of themain phyletic groups represented in marine andfreshwater systems. In addition Reynolds reviewsrecent advances in community ecology, developingan appreciation of assembly processes, coexistenceand competition, disturbance and diversity. Aimedprimarily at students of the plankton, it developsmany concepts relevant to ecology in the widestsense, and as such will appeal to a wide readershipamong students of ecology, limnology and oceanog-raphy.

Born in London, Colin completed his formal edu-cation at Sir John Cass College, University of Lon-don. He worked briefly with the Metropolitan Water

Board and as a tutor with the Field Studies Coun-cil. In 1970, he joined the staff at the WindermereLaboratory of the Freshwater Biological Association.He studied the phytoplankton of eutrophic meres,then on the renowned Lund Tubes, the large lim-netic enclosures in Blelham Tarn, before turning hisattention to the phytoplankton of rivers. During the1990s, working with Dr Tony Irish and, later, also DrAlex Elliott, he helped to develop a family of modelsbased on, the dynamic responses of phytoplanktonpopulations that are now widely used by managers.He has published two books, edited a dozen othersand has published over 220 scientific papers aswell as about 150 reports for clients. He hasgiven advanced courses in UK, Germany, Argentina,Australia and Uruguay. He was the winner of the1994 Limnetic Ecology Prize; he was awarded a cov-eted NaumannThienemann Medal of SIL and washonoured by Her Majesty the Queen as a Member ofthe British Empire. Colin also served on his munici-pal authority for 18 years and was elected mayor ofKendal in 199293.

e c o l o g y, b i o d i v e r s i t y, a n d c o n s e r va t i o n

Series editors

Michael Usher University of Stirling, and formerly Scottish Natural HeritageDenis Saunders Formerly CSIRO Division of Sustainable Ecosystems, CanberraRobert Peet University of North Carolina, Chapel HillAndrew Dobson Princeton University

Editorial BoardPaul Adam University of New South Wales, AustraliaH. J. B. Birks University of Bergen, NorwayLena Gustafsson Swedish University of Agricultural ScienceJeff McNeely International Union for the Conservation of NatureR. T. Paine University of WashingtonDavid Richardson University of Cape TownJeremy Wilson Royal Society for the Protection of Birds

The worlds biological diversity faces unprecedented threats. The urgent challenge facing the con-cerned biologist is to understand ecological processes well enough to maintain their functioning inthe face of the pressures resulting from human population growth. Those concerned with the con-servation of biodiversity and with restoration also need to be acquainted with the political, social,historical, economic and legal frameworks within which ecological and conservation practice mustbe developed. This series will present balanced, comprehensive, up-to-date and critical reviews ofselected topics within the sciences of ecology and conservation biology, both botanical and zoo-logical, and both pure and applied. It is aimed at advanced (final-year undergraduates, graduatestudents, researchers and university teachers, as well as ecologists and conservationists in indus-try, government and the voluntary sectors. The series encompasses a wide range of approaches andscales (spatial, temporal, and taxonomic), including quantitative, theoretical, population, community,ecosystem, landscape, historical, experimental, behavioural and evolutionary studies. The emphasisis on science related to the real world of plants and animals, rather than on purely theoreticalabstractions and mathematical models. Books in this series will, wherever possible, consider issuesfrom a broad perspective. Some books will challenge existing paradigms and present new ecologicalconcepts, empirical or theoretical models, and testable hypotheses. Other books will explore newapproaches and present syntheses on topics of ecological importance.Ecology and Control of Introduced Plants Judith H. Myers and Dawn R. BazelyInvertebrate Conservation and Agricultural Ecosystems T. R. NewRisks and Decisions for Conservation and Environmental Management Mark BurgmanNonequilibrium Ecology Klaus RohdeEcology of Populations Esa Ranta, Veijo Kaitala and Per Lundberg

The Ecology of Phytoplankton

C. S. Reynolds

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This book is dedicated tomy wife, JEAN, to whom its writingrepresented an intrusion intodomestic life, and to Charles Sinker,John Lund and Ramon Margalef. Each isa constant source of inspiration to me.

Contents

Preface page ix

Acknowledgements xii

Chapter 1. Phytoplankton 11.1 Definitions and terminology 1

1.2 Historical context of phytoplankton studies 3

1.3 The diversification of phytoplankton 4

1.4 General features of phytoplankton 15

1.5 The construction and composition of freshwater

phytoplankton 24

1.6 Marine phytoplankton 34

1.7 Summary 36

Chapter 2. Entrainment and distribution in the pelagic 382.1 Introduction 38

2.2 Motion in aquatic environments 39

2.3 Turbulence 42

2.4 Phytoplankton sinking and floating 49

2.5 Adaptive and evolutionary mechanisms for

regulating ws 53

2.6 Sinking and entrainment in natural turbulence 67

2.7 The spatial distribution of phytoplankton 77

2.8 Summary 90

Chapter 3. Photosynthesis and carbon acquisition inphytoplankton 933.1 Introduction 93

3.2 Essential biochemistry of photosynthesis 94

3.3 Light-dependent environmental sensitivity of

photosynthesis 101

3.4 Sensitivity of aquatic photosynthesis to carbon

sources 124

3.5 Capacity, achievement and fate of primary

production at the ecosystem scale 131

3.6 Summary 143

Chapter 4. Nutrient uptake and assimilation inphytoplankton 1454.1 Introduction 145

4.2 Cell uptake and intracellular transport of

nutrients 146

4.3 Phosphorus: requirements, uptake, deployment in

phytoplankton 151

viii CONTENTS

4.4 Nitrogen: requirements, sources, uptake and

metabolism in phytoplankton 161

4.5 The role of micronutrients 166

4.6 Major ions 171

4.7 Silicon: requirements, uptake, deployment in

phytoplankton 173

4.8 Summary 175

Chapter 5. Growth and replication of phytoplankton 1785.1 Introduction: characterising growth 178

5.2 The mechanics and control of growth 179

5.3 The dynamics of phytoplankton growth and

replication in controlled conditions 183

5.4 Replication rates under sub-ideal conditions 189

5.5 Growth of phytoplankton in natural

environments 217

5.6 Summary 236

Chapter 6. Mortality and loss processes in phytoplankton 2396.1 Introduction 239

6.2 Wash-out and dilution 240

6.3 Sedimentation 243

6.4 Consumption by herbivores 250

6.5 Susceptibility to pathogens and parasites 292

6.6 Death and decomposition 296

6.7 Aggregated impacts of loss processes on

phytoplankton composition 297

6.8 Summary 300

Chapter 7. Community assembly in the plankton: pattern,process and dynamics 3027.1 Introduction 302

7.2 Patterns of species composition and temporal

change in phytoplankton assemblages 302

7.3 Assembly processes in the phytoplankton 350

7.4 Summary 385

Chapter 8. Phytoplankton ecology and aquatic ecosystems:mechanisms and management 3878.1 Introduction 387

8.2 Material transfers and energy flow in pelagic

systems 387

8.3 Anthropogenic change in pelagic environments 395

8.4 Summary 432

8.5 A last word 435

Glossary 437

Units, symbols and abbreviations 440

CONTENTS ix

References 447

Index to lakes, rivers and seas 508

Index to genera and species ofphytoplankton 511

Index to genera and species of otherorganisms 520

General index 524

Preface

This is the third book I have written on the sub-ject of phytoplankton ecology. When I finishedthe first, The Ecology of Freshwater Phytoplankton(Reynolds, 1984a), I vowed that it would also bemy last. I felt better about it once it was pub-lished but, as I recognised that science was mov-ing on, I became increasingly frustrated aboutthe growing datedness of its information. Whenan opportunity was presented to me, in the formof the 1994 Ecology Institute Prize, to write mysecond book on the ecology of plankton, Vege-tation Processes in the Pelagic (Reynolds, 1997a), Iwas able to draw on the enormous strides thatwere being made towards understanding the partplayed by the biochemistry, physiology and pop-ulation dynamics of plankton in the overall func-tioning of the great aquatic ecosystems. Any feel-ing of satisfaction that that exercise brought tome has also been overtaken by events of the lastdecade, which have seen new tools deployed tothe greater amplification of knowledge and newfacts uncovered to be threaded into the web ofunderstanding of how the world works.

Of course, this is the way of science. Thereis no scientific text that can be closed with asigh, So thats it, then. There are always morequestions. I actually have rather more now thanI had at the same stage of finishing the 1984 vol-ume. No, the best that can be expected, or evenhoped for, is a periodic stocktake: This is whatwe have learned, this is how we think we canexplain things and this is where it fits into whatwe thought we knew already; this will stand untilwe learn something else. This is truly the wayof science. Taking observations, verifying themby experimentation, moving from hypothesis tofact, we are able to formulate progressively closerapproximations to the truth.

In fact, the second violation of my 1984 vowhas a more powerful and less high-principleddriver. It is just that the progress in planktonecology since 1984 has been astounding, turningalmost each one of the first books basic assump-tions on its head. Besides widening the scope of

the present volume to address more overtly themarine phytoplankton, I have set out to constructa new perspective on the expanded knowledgebase. I have to say at once that the omission offreshwater from the new title does not implythat the book covers the ecology of marine plank-ton in equivalent detail. It does, however, signifya genuine attempt to bridge the deep but whollyartificial chasm that exists between marine andfreshwater science, which political organisationand science funding have perpetuated.

At a personal level, this wider view is a satisfy-ing thing to develop, being almost a plea for abso-lution I am sorry for getting it wrong before,this is what I should have said! At a wider level, Iam conscious that many people still use and fre-quently cite my 1984 book; I would like them toknow that I no longer believe everything, or evenvery much, of what I wrote then. As if to empha-sise this, I have adopted a very similar approachto the subject, again using eight chapters (albeitwith altered titles). These are developed accord-ing to a similar sequence of topics, through mor-phology, suspension, ecophysiology and dynam-ics to the structuring of communities and theirfunctions within ecosystems. This arrangementallows me to contrast directly the new knowl-edge and the understanding it has renderedredundant.

So just what are these mould-breakingfindings? In truth, they impinge upon the sub-ject matter in each of the chapters. Advances inmicroscopy have allowed ultrastructural detailsof planktic organisms to be revealed for the firsttime. The advances in molecular biology, in par-ticular the introduction of techniques for iso-lating chromosomes and ribosomes, fragmentingthem by restriction enzymes and reading geneticsequences, have totally altered perceptions aboutphyletic relationships among planktic taxa andsuppositions about their evolution. The classifica-tion of organisms is undergoing change of revolu-tionary proportions, while morphological varia-tion among (supposedly) homogeneous genotypes

xii PREFACE

questions the very concept of putting namesto individual organisms. At the scale of cells,the whole concept of how they are moved inthe water has been addressed mathematically.It is now appreciated that planktic cells experi-ence critical physical forces that are very differ-ent from those affecting (say) fish: viscosity andsmall-scale turbulence determine the immediateenvironment of microorganisms; surface tensionis a lethal and inescapable spectre; while shearforces dominate dispersion and the spatial dis-tributions of populations. These discoveries flowfrom the giant leaps in quantification and mea-surements made by physical limnologists andoceanographers since the early 1980s. These havealso impinged on the revision of how sinkingand settlement of phytoplankton are viewed andthey have helped to consolidate a robust theoryof filter-feeding by zooplankton.

The way in which nutrients are sequesteredfrom dilute and dispersed sources in the waterand then deployed in the assembly and replica-tion of new generations of phytoplankton hasbeen intensively investigated by physiologists.Recent findings have greatly modified percep-tions about what is meant by limiting nutrientsand what happens when one or other is in shortsupply. As Sommer (1996) commented, past sup-positions about the repercussions on communitystructure have had to be revised, both throughthe direct implications for interspecific compe-tition for resources and, indirectly, through theeffects of variable nutritional value of potentialfoods to the web of dependent consumers.

Arguably, the greatest shift in understandingconcerns the way in which the pelagic ecosys-tem works. Although the abundance of plank-tic bacteria and the relatively vast reserve ofdissolved organic carbon (DOC) had long beenrecognised, the microorganismic turnover of car-bon has only been investigated intensively dur-ing the last two decades. It was soon recog-nised that the metazoan food web of the openoceans is linked to the producer network viathe turnover of the microbes and that this state-ment applies to many larger freshwater systemsas well. The metabolism of the variety of sub-stances embraced by DOC varies with source andchain length but a labile fraction originates from

phytoplankton photosynthesis that is leaked oractively discharged into the water. Far from hold-ing to the traditional view of the pelagic foodchain algae, zooplankton, fish plankton ecol-ogists now have to acknowledge that marinefood webs are regulated by a sea of microbes(Karl, 1999), through the muliple interactions oforganic and inorganic resources and by the lockof protistan predators and acellular pathogens(Smetacek, 2002). Even in lakes, where the casefor the topdown control of phytoplankton byherbivorous grazers is championed, the other-wise dominant microbially mediated supply ofresources to higher trophic levels is demonstra-bly subsidised by components from the littoral(Schindler et al., 1996; Vadeboncoeur et al., 2002).

There have been many other revolutions. Onemore to mention here is the progress in ecosys-tem ecology, or more particularly, the bridgebetween the organismic and population ecologyand the behaviour of entire systems. How ecosys-tems behave, how their structure is maintainedand what is critical to that maintenance, whatthe biogeochemical consequences might be andhow they respond to human exploitation andmanagement, have all become quantifiable. Thelinking threads are based upon thermodynamicrules of energy capture, exergy storage and struc-tural emergence, applied through to the systemslevel (Link, 2002; Odum, 2002).

In the later chapters in this volume, I attemptto apply these concepts to phytoplankton-basedsystems, where the opportunity is again takento emphasise the value to the science of ecol-ogy of studying the dynamics of microorganismsin the pursuit of high-order pattern and assem-bly rules (Reynolds, 1997, 2002b). The dual chal-lenge remains, to convince students of forestsand other terrestrial ecosystems that microbialsystems do conform to analogous rules, albeitat very truncated real-time scales, and to per-suade microbiologists to look up from the micro-scope for long enough to see how their knowl-edge might be applied to ecological issues.

I am proud to acknowledge the many peoplewho have influenced or contributed to the sub-ject matter of this book. I thank Charles Sinkerfor inspiring a deep appreciation of ecology andits mechanisms. I am grateful to John Lund, CBE,

PREFACE xiii

FRS for the opportunity to work on phytoplank-ton as a postgraduate and for the constant inspi-ration and access to his knowledge that he hasgiven me. Of the many practising theoretical ecol-ogists whose works I have read, I have felt thegreatest affinity to the ideas and logic of RamonMargalef; I greatly enjoyed the opportunities todiscuss these with him and regret that there willbe no more of them.

I gratefully acknowledge the various scien-tists whose work has profoundly influenced par-ticular parts of this book and my thinking gen-erally. They include (in alphabetical order) Sal-lie Chisholm, Paul Falkowski, Maciej Gliwicz,Phil Grime, Alan Hildrew, G. E. Hutchinson, JorgImberger, Petur Jonasson, Sven-Erik Jrgensen,Dave Karl, Winfried Lampert, John Lawton, JohnRaven, Marten Scheffer, Ted Smayda, MilanStraskraba, Reinhold Tuxen, Anthony Walsby andThomas Weisse. I have also been most fortu-nate in having been able, at various times, towork with and discuss many ideas with col-leagues who include Keith Beven, Sylvia Bonilla,Odcio Caceres, Paul Carling, Jean-Pierre Descy,Monica Diaz, Graham Harris, Vera Huszar, DieterImboden, Kana Ishikawa, Medina Kadiri, SusanKilham, Michio Kumagai, Bill Li, Vivian Monte-cino, Mohi Munawar, Masami Nakanishi, Shin-Ichi Nakano, Luigi Naselli-Flores, Pat Neale, SrenNielsen, Judit Padisak, Fernando Pedrozo, VictorSmetacek, Ulrich Sommer, Jos Tundisi andPeter Tyler. I am especially grateful to Cather-ine Legrand who generously allowed me to useand interpret her experimental data on Alexan-drium. Nearer to home, I have similarly benefitedfrom long and helpful discussions with such erst-while Windermere colleagues as Hilda Canter-Lund, Bill Davison, Malcolm Elliott, Bland Finlay,Glen George, Ivan Heaney, Stephen Maberly, JackTalling and Ed Tipping.

During my years at The Ferry House, I wasably and closely supported by several co-workers,

among whom special thanks are due to TonyIrish, Sheila Wiseman, George Jaworski and BrianGodfrey. Peter Allen, Christine Butterwick, JulieCorry (later Parker), Mitzi De Ville, Joy Elsworth,Alastair Ferguson, Mark Glaister, David Gouldney,Matthew Rogers, Stephen Thackeray and JulieThompson also worked with me at particulartimes. Throughout this period, I was privilegedto work in a well-found laboratory with abun-dant technical and practical support. I freelyacknowledge use of the worlds finest collectionof the freshwater literature and the assistanceprovided at various times by John Horne, IanPettman, Ian McCullough, Olive Jolly and Mari-lyn Moore. Secretarial assistance has come fromMargaret Thompson, Elisabeth Evans and JoyceHawksworth. Trevor Furnass has provided abun-dant reprographic assistance over many years. Iam forever in the debt of Hilda Canter-Lund, FRPSfor the use of her internationally renowned pho-tomicrographs.

A special word is due to the doctoral studentswhom I have supervised. The thirst for knowl-edge and understanding of a good pupil gener-ally provide a foil and focus in the other direc-tion. I owe much to the diligent curiosity of Chrisvan Vlymen, Helena Cmiech, Karen Saxby (nowRouen), Sian Davies, Alex Elliott, Carla Kruk andPhil Davis.

My final word of appreciation is reserved foracknowledgement of the tolerance and forbear-ance of my wife and family. I cheered throughmany juvenile football matches and dutifullyattended a host of ballet and choir performancesand, yes, it was quite fun to relive three moreschool curricula. Nevertheless, my children hadless of my time than they were entitled to expect.Jean has generously shared with my science thefull focus of my attention. Yet, in 35 years of mar-riage, she has never once complained, nor doneless than encourage the pursuit of my work. I amproud to dedicate this book to her.

Acknowledgements

Except where stated, the illustrations in this bookare reproduced, redrawn or otherwise slightlymodified from sources noted in the individualcaptions. The author and the publisher are grate-ful to the various copyright holders, listed below,who have given permission to use copyright mate-rial in this volume. While every effort has beenmade to clear permissions as appropriate, thepublisher would appreciate notification of anyomission.

Figures 1.1 to 1.8, 1.10, 2.8 to 2.13, 2.17, 2.20 to2.31, 3.3 to 3.9, 3.16 and 3.17, 5.20, 6.2, 6.7, 6.11.7.6 and 7.18 are already copyrighted to CambridgeUniversity Press.

Figure 1.9 is redrawn by permission of OxfordUniversity Press.

Figure 1.11 is the copyright of the American Soci-ety of Limnology and Oceanography.

Figures 2.1 and 2.2, 2.5 to 2.7, 2.15 and 2.16, 2.18and 2.19, 3.12, 3.14, 3.19, 4.1, 4.3 to 4.5, 5.1 to5.5, 5.8, 5.10, 5.12 and 5.13, 5.20 and 5.21, 6.1,6.2, 6.4, 6.14, 7.8, 7.10 and 7.11, 7.14, 7.16 and 7.17,7.20 and 7.22 are redrawn by permission of TheEcology Institute, Oldendorf.

Figures 2.3 and 4.7 are redrawn from the sourcenoted in the captions, with acknowledgement toArtemis Press.

Figures 2.4, 3.18, 5.11, 5.18, 7.5, 7.15, 8.2 and 8.3are redrawn from the various sources noted inthe respective captions and with acknowledge-ment to Elsevier Science, B.V.

Figure 2.14 is redrawn from the British Phycologi-cal Journal by permission of Taylor & Francis Ltd(http://www.tandf.co.uk/journals).

Figure 3.1 is redrawn by permission of NaturePublishing Group.

Figures 3.2, 3.11, 3.13, 4.2, 5.6, 6.4, 6.6, 6.9,6.10 and 6.13 come from various titles that are

the copyright of Blackwell Science (the specificsources are noted in the figure captions) and areredrawn by permission.

Figures 3.7, 3.15, 4.6 and 7.2.3 (or parts thereof)are redrawn from Freshwater Biology by permissionof Blackwell Science.

Figure 3.7 incorporates items redrawn from Bio-logical Reviews with acknowledgement to the Cam-bridge Philosophical Society.

Figure 5.9 is redrawn by permission of John Wiley& Sons Ltd.

Figure 5.14 is redrawn by permission of Springer-Verlag GmbH.

Figures 5.15 to 5.17, 5.19, 6.8 and 6.9 are redrawnby permission of SpringerScience+Business BV.Figures 6.12, 6.15, 7.1 to 7.4, 7.9 and 8.6 are repro-duced from Journal of Plankton Research by permis-sion of Oxford University Press. Dr K. Bruning alsogave permission to produce Fig. 6.12.

Figure 7.7 is redrawn by permission of the Direc-tor, Marine Biological Association.

Figures 7.12 to 7.14, 7.24 and 7.25 are redrawnfrom Verhandlungen der internationale Vereini-gung fur theoretische und angewandte Limnolo-gie by permission of Dr E. Nagele (Publisher)(http://www.schwezerbart.de).

Figure 7.19 is redrawn with acknowledgement tothe Athlone Press of the University of London.

Figure 7.21 is redrawn from Aquatic EcosystemsHealth and Management by permission of Taylor& Francis, Inc. (http://www.taylorandfrancis.com).

Figure 8.1 is redrawn from Scientia Maritima bypermission of Institut de Cincies del Mar.

Figures 8.5, 8.7 and 8.8 are redrawn by permis-sion of the Chief Executive, Freshwater BiologicalAssociation.

Chapter 1

Phytoplankton

1.1 Definitions and terminology

The correct place to begin any exposition of amajor component in biospheric functioning iswith precise definitions and crisp discrimination.This should be a relatively simple exercise but forthe need to satisfy a consensus of understand-ing and usage. Particularly among the biologicalsciences, scientific knowledge is evolving rapidlyand, as it does so, it often modifies and outgrowsthe constraints of the previously acceptable ter-minology. I recognised this problem for plank-ton science in an earlier monograph (Reynolds,1984a). Since then, the difficulty has worsenedand it impinges on many sections of the presentbook. The best means of dealing with it is toaccept the issue as a symptom of the good healthand dynamism of the science and to avoid con-straining future philosophical development by aredundant terminological framework.

The need for definitions is not subverted, how-ever, but it transforms to an insistence that thosethat are ventured are provisional and, thus, opento challenge and change. To be able to revealsomething also of the historical context of theusage is to give some indication of the limitationsof the terminology and of the areas of conjectureimpinging upon it.

So it is with plankton. The general under-standing of this term is that it refers to the col-lective of organisms that are adapted to spend partor all of their lives in apparent suspension in theopen water of the sea, of lakes, ponds and rivers.The italicised words are crucial to the concept

and are not necessarily contested. Thus, plank-ton excludes other suspensoids that are eithernon-living, such as clay particles and precipitatedchemicals, or are fragments or cadavers derivedfrom biogenic sources. Despite the existence ofthe now largely redundant subdivision tychoplank-ton (see Box 1.1), plankton normally comprisesthose living organisms that are only fortuitouslyand temporarily present, imported from adjacenthabitats but which neither grew in this habitatnor are suitably adapted to survive in the trulyopen water, ostensibly independent of shore andbottom. Such locations support distinct suites ofsurface-adhering organisms with their own dis-tinctive survival adaptations.

Suspension has been more problematic, hav-ing quite rigid physical qualifications of dens-ity and movement relative to water. As will berehearsed in Chapter 2, only rarely can plank-ton be isopycnic (having the same density) withthe medium and will have a tendency to f loatupwards or sink downwards relative to it. Therate of movement is also size dependent, sothat apparent suspension is most consistentlyachieved by organisms of small (

2 PHYTOPLANKTON

Box 1.1 Some definitions used in the literaureon plankton

seston the totality of particulate matter in water; all material notin solution

tripton non-living sestonplankton living seston, adapted for a life spent wholly or partly in

quasi-suspension in open water, and whose powers ofmotility do not exceed turbulent entrainment (seeChapter 2)

nekton animals adapted to living all or part of their lives in openwater but whose intrinsic movements are almostindependent of turbulence

euplankton redundant term to distinguish fully adapted, truly plankticorganisms from other living organisms fortuitouslypresent in the water

tychoplankton non-adapted organisms from adjacent habitats andpresent in the water mainly by chance

meroplankton planktic organisms passing a major part of the life historyout of the plankton (e.g. on the bottom sediments)

limnoplankton plankton of lakesheleoplankton plankton of pondspotamoplankton plankton of riversphytoplankton planktic photoautotrophs and major producer of the

pelagicbacterioplankton planktic prokaryotesmycoplankton planktic fungizooplankton planktic metazoa and heterotrophic protistans

Some more, now redundant, terms

The terms nannoplankton, ultraplankton, -algae are older names for various smallersize categories of phytoplankton, eclipsed by the classification of Sieburth et al.(1978) (see Box 1.2).

In this way, plankton comprises organismsthat range in size from that of viruses (a few tensof nanometres) to those of large jellyfish (a metreor more). Representative organisms include bac-teria, protistans, fungi and metazoans. In thepast, it has seemed relatively straightforward toseparate the organisms of the plankton, bothinto broad phyletic categories (e.g. bacterioplank-ton, mycoplankton) or into similarly broad func-tional categories (photosynthetic algae of thephytoplankton, phagotrophic animals of the zoo-plankton). Again, as knowledge of the organ-

isms, their phyletic affinities and physiologicalcapabilities has expanded, it has become clearthat the divisions used hitherto do not pre-cisely coincide: there are photosynthetic bac-teria, phagotrophic algae and flagellates that takeup organic carbon from solution. Here, as in gen-eral, precision will be considered relevant andimportant in the context of organismic prop-erties (their names, phylogenies, their morpho-logical and physiological characteristics). On theother hand, the generic contributions to sys-tems (at the habitat or ecosystem scales) of the

HISTORICAL CONTEXT OF PHYTOPLANKTON STUDIES 3

photosynthetic primary producers, phagotrophicconsumers and heterotrophic decomposers maybe attributed reasonably but imprecisely to phyto-plankton, zooplankton and bacterioplankton.

The defintion of phytoplankton adopted forthis book is the collective of photosyntheticmicroorganisms, adapted to live partly or contin-uously in open water. As such, it is the photoau-totrophic part of the plankton and a major pri-mary producer of organic carbon in the pelagicof the seas and of inland waters. The distinctionof phytoplankton from other categories of plank-ton and suspended matter are listed in Box 1.1.

It may be added that it is correct to refer tophytoplankton as a singular term (phytoplank-ton is rather than phytoplankton are). A singleorganism is a phytoplanktont or (more ususally)phytoplankter. Incidentally, the adjective plank-tic is etymologically preferable to the more com-monly used planktonic.

1.2 Historical context ofphytoplankton studies

The first use of the term plankton is attributedin several texts (Ruttner, 1953; Hutchinson, 1967)to Viktor Hensen, who, in the latter half of thenineteenth century, began to apply quantitativemethods to gauge the distribution, abundanceand productivity of the microscopic organismsof the open sea. The monograph that is usuallycited (Hensen, 1887) is, in fact, rather obscureand probably not well read in recent times butSmetacek et al. (2002) have provided a probingand engaging review of the original, within thecontext of early development of plankton science.Most of the present section is based on theirarticle.

The existence of a planktic community oforganisms in open water had been demonstratedmany years previously by Johannes Muller. Knowl-edge of some of the organisms themselvesstretches further back, to the earliest daysof microscopy. From the 1840s, Muller woulddemonstrate net collections to his students, usingthe word Auftrieb to characterise the commu-nity (Smetacek et al., 2002). The literal transla-

tion to English is up drive, approximately buoy-ancy or flotation, a clear reference to Mullersassumption that the material floated up to thesurface waters like so much oceanic dirt! Ittook one of Mullers students, Ernst Haeckel, tochampion the beauty of planktic protistans andmetazoans. His monograph on the Radiolariawas also one of the first to embrace Darwins(1859) evolutionary theory in order to showstructural affinities and divergences. Haeckel, ofcourse, became best known for his work onmorphology, ontogeny and phylogeny. Accordingto Smetacek et al. (2002), his interest and skillsas a draughtsman advanced scientific awarenessof the range of planktic form (most significantly,Haeckel, 1904) but to the detriment of any realprogress in understanding of functional differen-tiation. Until the late 1880s, it was not appreci-ated that the organisms of the Auftrieb, even thealgae among them, could contribute much to thenutrition of the larger animals of the sea. Instead,it seems to have been supposed that organic mat-ter in the fluvial discharge from the land was themajor nutritive input. It is thus rather interest-ing to note that, a century or so later, this pos-sibility has enjoyed something of a revival (seeChapters 3 and 8).

If Haeckel had conveyed the beauty of thepelagic protistans, it was certainly Viktor Hensenwho had been more concerned about their rolein a functional ecosystem. Hensen was a phys-iologist who brought a degree of empiricismto his study of the perplexing fluctuations inNorth Sea fish stocks. He had reasoned thatfish stocks and yields were related to the pro-duction and distribution of the juvenile stages.Through devising techniques for sampling, quan-tification and assessing distribution patterns,always carefully verified by microscopic exami-nation, Hensen recognised both the ubiquity ofphytoplankton and its superior abundance andquality over coastal inputs of terrestrial detritus.He saw the connection between phytoplanktonand the light in the near-surface layer, the nutri-tive resource it provided to copepods and othersmall animals, and the value of these as a foodsource to fish.

Thus, in addition to bequeathing a newname for the basal biotic component in pelagic

4 PHYTOPLANKTON

ecosystems, Hensen may be regarded justifiablyas the first quantitative plankton ecologist andas the person who established a formal method-ology for its study. Deducing the relative contri-butions of Hensen and Haeckel to the founda-tion of modern plankton science, Smetacek et al.(2002) concluded that it is the work of the lat-ter that has been the more influential. This is anopinion with which not everyone will agree butthis is of little consequence. However, Smetaceket al. (2002) offered a most profound and resonantobservation in suggesting that Hensens generalunderstanding of the role of plankton (the bigpicture) was essentially correct but erroneous inits details, whereas in Haeckels case, it was theother way round. Nevertheless, both have goodclaim to fatherhood of plankton science!

1.3 The diversification ofphytoplankton

Current estimates suggest that between 4000 and5000 legitimate species of marine phytoplank-ton have been described (Sournia et al. 1991;Tett and Barton, 1995). I have not seen a com-parable estimate for the number of species ininland waters, beyond the extrapolation I made(Reynolds, 1996a) that the number is unlikely tobe substantially smaller. In both lists, there isnot just a large number of mutually distinct taxaof photosynthetic microorganisms but there is awide variety of shape, size and phylogenetic affin-ity. As has also been pointed out before (Reynolds,1994a), the morphological range is comparable tothe one spanning forest trees and the herbs thatgrow at their base. The phyletic divergence of therepresentatives is yet wider. It would be surpris-ing if the species of the phytoplankton were uni-form in their requirements, dynamics and sus-ceptibilities to loss processes. Once again, thereis a strong case for attempting to categorise thephytoplankton both on the phylogeny of organ-isms and on the functional basis of their roles inaquatic ecosystems. Both objectives are adoptedfor the writing of this volume. Whereas the for-mer is addressed only in the present chapter, the

latter quest occupies most of the rest of the book.However, it is not giving away too much to antici-pate that systematics provides an important foun-dation for species-specific physiology and whichis itself part-related to morphology. Accordingly,great attention is paid here to the differentia-tion of individualistic properties of representa-tive species of phytoplankton.

However, there is value in being able simul-taneously to distinguish among functional cate-gories (trees from herbs!). The scaling system andnomenclature proposed by Sieburth et al. (1978)has been widely adopted in phytoplankton ecol-ogy to distinguish functional separations withinthe phytoplankton. It has also eclipsed the use ofsuch terms as -algae and ultraplankton to separatethe lower size range of planktic organisms fromthose (netplankton) large enough to be retainedby the meshes of a standard phytoplankton net.The scheme of prefixes has been applied to sizecategories of zooplankton, with equal success.The size-based categories are set out in Box 1.2.

At the level of phyla, the classification ofthe phytoplankton is based on long-standing cri-teria, distinguished by microscopists and bio-chemists over the last 150 years or so, fromwhich there is little dissent. In contrast, subdi-vision within classes, orders etc., and the tracingof intraphyletic relationships, affinities withinand among families, even the validity of suppos-edly well-characterised species, has become sub-ject to massive reappraisal. The new factor thathas come into play is the powerful armoury ofthe molecular biologists, including the methodsfor reading gene sequences and for the statisti-cal matching of these to measure the closenessto other species.

Of course, the potential outcome is a muchmore robust, genetically verified family tree ofauthentic species of phytoplankton. This may besome years away. For the present, it seems point-less to reproduce a detailed classification of thephytoplankton that will soon be made redun-dant. Even the evolutionary connectivities amongthe phyla and their relationship to the geochem-ical development of the planetary structuresare undergoing deep re-evaluation (Delwiche,2000; Falkowski, 2002). For these reasons, the

THE DIVERSIFICATION OF PHYTOPLANKTON 5

Box 1.2 The classification of phytoplankton according tothe scaling nomenclature of Sieburth et al. (1978)

Maximum linear dimension Namea

0.22 m picophytoplankton220 m nanophytoplankton20200 m microphytoplankton200 m2 mm mesophytoplankton>2 mm macrophytoplankton

aThe prefixes denote the same size categories when used with -zooplankton, -algae, -cyanobacteria,flagellates, etc.

taxonomic listings in Table 1.1 are deliberatelyconservative.

Although the life forms of the planktoninclude acellular microorganisms (viruses) and arange of well-characterised Archaea (the halobac-teria, methanogens and sulphur-reducing bac-teria, formerly comprising the Archaebacteria),the most basic photosynthetic organisms of thephytoplankton belong to the Bacteria (formerly,Eubacteria). The separation of the ancestral bac-teria from the archaeans (distinguished by thepossession of membranes formed of branchedhydrocarbons and ether linkages, as opposed tothe straight-chain fatty acids and ester linkagesfound in the membranes of all other organisms:Atlas and Bartha, 1993) occurred early in micro-bial evolution (Woese, 1987; Woese et al., 1990).

The appearance of phototrophic forms, dis-tinguished by their crucial ability to use lightenergy in order to synthesise adenosine triphos-phate (ATP) (see Chapter 3), was also an ancientevent that took place some 3000 million years ago(3 Ga BP (before present)). Some of these organ-isms were photoheterotrophs, requiring organicprecursors for the synthesis of their own cells.Modern forms include green flexibacteria (Chlo-roflexaceae) and purple non-sulphur bacteria(Rhodospirillaceae), which contain pigments sim-ilar to chlorophyll (bacteriochlorophyll a, b orc). Others were true photoautotrophs, capableof reducing carbon dioxide as a source of cellcarbon (photosynthesis). Light energy is used tostrip electrons from a donor substance. In most

modern plants, water is the source of reductantelectrons and oxygen is liberated as a by-product(oxygenic photosynthesis). Despite their phyleticproximity to the photoheterotrophs and shar-ing a similar complement of bacteriochloro-phylls (Bj et al., 2002), the Anoxyphotobac-teria use alternative sources of electrons and,in consequence, generate oxidation productsother than oxygen (anoxygenic photosynthesis).Their modern-day representatives are the purpleand green sulphur bacteria of anoxic sediments.Some of these are planktic in the sense thatthey inhabit anoxic, intensively stratified layersdeep in small and suitably stable lakes. The traitmight be seen as a legacy of having evolved in awholly anoxic world. However, aerobic, anoxy-genic phototrophic bacteria, containing bac-terichlorophyll a, have been isolated from oxicmarine environments (Shiba et al., 1979); it hasalso become clear that their contribution to theoceanic carbon cycle is not necessarily insignifi-cant (Kolber et al., 2001; Goericke, 2002).

Nevertheless, the oxygenic photosynthesis pio-neered by the Cyanobacteria from about 2.8 Gabefore present has proved to be a crucial step inthe evolution of life in water and, subsequently,on land. Moreover, the composition of the atmos-phere was eventually changed through the biolo-gical oxidation of water and the simultaneousremoval and burial of carbon in marine sedi-ments (Falkowski, 2002). Cyanobacterial photo-synthesis is mediated primarily by chlorophylla, borne on thylakoid membranes. Accessory

6 PHYTOPLANKTON

Table 1.1 Survey of the organisms in the phytoplankton

Domain: BACTERIADivision: Cyanobacteria (blue-green algae)

Unicellular and colonial bacteria, lacking membrane bound plastids. Primaryphotosynthetic pigment is chlorophyll a, with accessory phycobilins (phycocyanin,phycoerythrin). Assimilation products, glycogen, cyanophycin. Four main sub-groups,of which three have planktic representatives.

Order: CHROOCOCCALESUnicellular or coenobial Cyanobacteria but never filamentous. Most planktic generaform mucilaginous colonies, and these are mainly in fresh water. Picophytoplankticforms abundant in the oceans.

Includes: Aphanocapsa, Aphanothece, Chroococcus, Cyanodictyon,Gomphosphaeria, Merismopedia, Microcystis, Snowella, Synechococcus,Synechocystis, Woronichinia

Order: OSCILLATORIALESUniseriatefilamentous Cyanobacteria whose cells all undergo division in the sameplane. Marine and freshwater genera.

Includes: Arthrospira, Limnothrix, Lyngbya, Planktothrix, Pseudanabaena, Spirulina,Trichodesmium, Tychonema

Order: NOSTOCALESUnbranchedfilamentous Cyanobacteria whose cells all undergo division in the sameplane and certain of which may be facultatively differentiated into heterocysts. In theplankton of fresh waters and dilute seas.

Includes: Anabaena, Anabaenopsis, Aphanizomenon, Cylindrospermopsis,Gloeotrichia, Nodularia

Exempt Division: ProchlorobacteriaOrder: PROCHLORALES

Unicellular and colonial bacteria, lacking membrane-bound plastids. Photosyntheticpigments are chlorophyll a and b, but lack phycobilins.

Includes: Prochloroccus, Prochloron, ProchlorothrixDivision: Anoxyphotobacteria

Mostly unicellular bacteria whose (anaerobic) photosynythesis depends upon anelectron donor other than water and so do not generate oxygen. Inhabit anaerobicsediments and (where appropriate) water layers where light penetrates sufficiently.Two main groups:

Family: Chromatiaceae (purple sulphur bacteria) Cells able to photosynthesisewith sulphide as sole electron donor. Cells contain bacteriochlorophyll a, b or c.

Includes: Chromatium, Thiocystis, Thiopedia.Family: Chlorobiaceae (green sulphur bacteria) Cells able to photosynthesisewith sulphide as sole electron donor. Cells contain bacteriochlorophyll a, b or c.

Includes: Chlorobium, Clathrocystis, Pelodictyon.Domain: EUCARYA

Phylum: GlaucophytaCyanelle-bearing organisms, with freshwater planktic representatives.

Includes: Cyanophora, Glaucocystis.Phylum: Prasinophyta

Unicellular, mostly motile green algae with 116 laterally or apically placed flagella,cell walls covered with fine scales and plastids containing chlorophyll a and b.Assimilatory products mannitol, starch.

(cont.)

THE DIVERSIFICATION OF PHYTOPLANKTON 7

Table 1.1 (cont.)

CLASS: PedinophyceaeOrder: PEDINOMONADALES

Small cells, with single lateral flagellum.Includes: Pedinomonas

CLASS: PrasinophyceaeOrder: CHLORODENDRALES

Flattened, 4-flagellated cells.Includes: Nephroselmis, Scherffelia (freshwater); Mantoniella, Micromonas(marine)

Order: PYRAMIMONADALESCells with 4 or 8 (rarely 16) flagella arising from an anterior depression. Marineand freshwater.

Includes: PyramimonasOrder: SCOURFIELDIALES

Cells with two, sometimes unequal, flagella. Known from freshwater ponds.Includes: Scourfieldia

Phylum: Chlorophyta (green algae)Green-pigmented, unicellular, colonial, filamentous, siphonaceous and thalloidalgae. One or more chloroplasts containing chlorophyll a and b. Assimilationproduct, starch (rarely, lipid).

CLASS: ChlorophyceaeSeveral orders of which the following have planktic representatives:

Order: TETRASPORALESNon-flagellate cells embedded in mucilaginous or palmelloid colonies, but withmotile propagules.

Includes: Paulschulzia, PseudosphaerocystisOrder: VOLVOCALES

Unicellular or colonial biflagellates, cells with cup-shaped chloroplasts.Includes: Chlamydomonas, Eudorina, Pandorina, Phacotus, Volvox (in freshwaters); Dunaliella, Nannochloris (marine)

Order: CHLOROCOCCALESNon-flagellate, unicellular or coenobial (sometimes mucilaginous) algae, withmany planktic genera.

Includes: Ankistrodesmus, Ankyra, Botryococcus, Chlorella,Coelastrum, Coenochloris, Crucigena, Choricystis, Dictyosphaerium,Elakatothrix, Kirchneriella, Monorophidium, Oocystis, Pediastrum,Scenedesmus, Tetrastrum

Order: ULOTRICHALESUnicellular or mostly unbranched filamentous with band-shaped chloroplasts.

Includes: Geminella, Koliella, StichococcusOrder: ZYGNEMATALES

Unicellular or filamentous green algae, reproducing isogamously by conjugation.Planktic genera are mostly members of the Desmidaceae, mostly unicellular or(rarely) filmentous coenobia with cells more or less constricted into twosemi-cells linked by an interconnecting isthmus. Exclusively freshwater genera.

Includes: Arthrodesmus, Closterium, Cosmarium, Euastrum, Spondylosium,Staurastrum, Staurodesmus, Xanthidium

(cont.)

8 PHYTOPLANKTON

Table 1.1 (cont.)

Phylum: EuglenophytaGreen-pigmented unicellular biflagellates. Plastids numerous and irregular,containing chlorophyll a and b. Reproduction by longitudinal fission. Assimilationproduct, paramylon, oil. One Class, Euglenophyceae, with two orders.

Order: EUTREPTIALESCells having two emergent flagella, of approximately equal length. Marine andfreshwater species.

Includes: EutreptiaOrder: EUGLENALES

Cells having two flagella, one very short, one long and emergent.Includes: Euglena, Lepocinclis, Phacus, Trachelmonas

Phylum: CryptophytaOrder: CRYPTOMONADALES

Naked, unequally biflagellates with one or two large plastids, containingchlorophyll a and c2 (but not chlorophyll b); accessory phycobiliproteins or otherpigments colour cells brown, blue, blue-green or red; assimilatory product,starch. Freshwater and marine species.

Includes: Chilomonas, Chroomonas, Cryptomonas, Plagioselmis, Pyrenomonas,Rhodomonas

Phylum: RaphidophytaOrder: RAPHIDOMONADALES (syn. CHLOROMONADALES)

Biflagellate, cellulose-walled cells; two or more plastids containing chlorophyll a;cells yellow-green due to predominant accessory pigment, diatoxanthin;assimilatory product, lipid. Freshwater.

Includes: GonyostomumPhylum: Xanthophyta (yellow-green algae)

Unicellular, colonial, filamentous and coenocytic algae. Motile species generallysubapically and unequally biflagellated; two or many more discoid plastids per cellcontaining chlorophyll a. Cells mostly yellow-green due to predominantaccessory pigment, diatoxanthin; assimilation product, lipid. Several orders, twowith freshwater planktic representatives.

Order: MISCHOCOCCALESRigid-walled, unicellular, sometimes colonial xanthophytes.

Includes: Goniochloris, Nephrodiella, OphiocytiumOrder: TRIBONEMATALES

Simple or branched uniseriate filamentous xanthophytes.Includes: Tribonema

Phylum: EustigmatophytaCoccoid unicellular, flagellated or unequally biflagellated yellow-green algae withmasking of chlorophyll a by accessory pigment violaxanthin. Assimilation product,probably lipid.

Includes: Chlorobotrys, MonodusPhylum: Chrysophyta (golden algae)

Unicellular, colonial and filamentous. often uniflagellate, or unequally biflagellatealgae. Contain chlorophyll a, c1 and c2, generally masked by abundant accessorypigment, fucoxanthin, imparting distinctive golden colour to cells. Cellssometimes naked or or enclosed in an urn-shaped lorica, sometimes withsiliceous scales. Assimilation products, lipid, leucosin. Much reclassified group, hasseveral classes and orders in the plankton.

(cont.)

THE DIVERSIFICATION OF PHYTOPLANKTON 9

Table 1.1 (cont.)

CLASS: ChrysophyceaeOrder: CHROMULINALES

Mostly planktic, unicellular or colony-forming flagellates with one or twounequal flagella, occasionally naked, often in a hyaline lorica or gelatinousenvelope.

Includes: Chromulina, Chrysococcus, Chrysolykos, Chrysosphaerella, Dinobryon,Kephyrion, Ochromonas, Uroglena

Order: HIBBERDIALESUnicellular or colony-forming epiphytic gold algae but some plankticrepresentatives.

Includes: BitrichiaCLASS: DictyochophyceaeOrder: PEDINELLALES

Radially symmetrical, very unequally biflagellate unicells or coenobia.Includes: Pedinella (freshwater); Apedinella, Pelagococcus, Pelagomonas,Pseudopedinella (marine)

CLASS: SynurophyceaeOrder: SYNURALES

Unicellular or colony-forming flagellates, bearing distinctive siliceous scales.Includes: Mallomonas, Synura

Phylum: Bacillariophyta (diatoms)Unicellular and coenobial yellow-brown, non-motile algae with numerous discoidplastids, containing chlorophyll a, c1 and c2, masked by accessory pigment,fucoxanthin. Cell walls pectinaceous, in two distinct and overlapping halves, andimpregnated with cryptocrystalline silica. Assimilatory products, chrysose, lipids.Two large orders, both conspicuously represented in the marine and freshwaterphytoplankton.

CLASS: BacillariophyceaeOrder: BIDDULPHIALES (centric diatoms)

Diatoms with cylindrical halves, sometimes well separated by girdle bands. Somespecies form (pseudo-)filaments by adhesion of cells at their valve ends.

Includes: Aulacoseira, Cyclotella, Stephanodiscus, Urosolenia (freshwater);Cerataulina, Chaetoceros, Detonula, Rhizosolenia, Skeletonema, Thalassiosira(marine)

Order: BACILLARIALES (pennate diatoms)Diatoms with boat-like halves, no girdle bands. Some species form coenobia byadhesion of cells on their girdle edges.

Includes: Asterionella, Diatoma, Fragilaria, Synedra, Tabellaria (freshwater);Achnanthes, Fragilariopsis, Nitzschia (marine)

Phylum: HaptophytaCLASS: Haptophyceae

Gold or yellow-brown algae, usually unicellular, with two subequal flagella and acoiled haptonema, but with amoeboid, coccoid or palmelloid stages. Pigments,chlorophyll a, c1 and c2, masked by accessory pigment (usually fucoxanthin).Assimilatory product, chrysolaminarin. Cell walls with scales, sometimes more orless calcified.

Order: PAVLOVALESCells with haired flagella and small haptonema. Marine and freshwater species.

Includes: Diacronema, Pavlova(cont.)

10 PHYTOPLANKTON

Table 1.1 (cont.)

Order: PRYMNESIALESCells with smooth flagella, haptonema usually small. Mainly marine or brackishbut some common in freshwater plankton.

Includes: Chrysochromulina, Isochrysis, Phaeocystis, PrymnesiumOrder: COCCOLITHOPHORIDALES

Cell suface covered by small, often complex, flat calcified scales (coccoliths).Exclusively marine.

Include: Coccolithus, Emiliana, Florisphaera, Gephyrocapsa, UmbellosphaeraPhylum: Dinophyta

Mostly unicellular, sometimes colonial, algae with two flagella of unequal lengthand orientation. Complex plastids containing chlorophyll a, c1 and c2, generallymasked by accessory pigments. Cell walls firm, or reinforced with polygonalplates. Assimilation products: starch, oil. Conspicuously represented in marineand freshwater plankton. Two classes and (according to some authorities) up to11 orders.

CLASS: DinophyceaeBiflagellates, with one transverse flagellum encircling the cell, the other directedposteriorly.

Order: GYMNODINIALESFree-living, free-swimming with flagella located in well-developed transverse andsulcal grooves, without thecal plates. Mostly marine.

Includes: Amphidinium, Gymnodinium, WoloszynskiaOrder: GONYAULACALES

Armoured, plated, free-living unicells, the apical plates being asymmetrical.Marine and freshwater.

Includes: Ceratium, LingulodiniumOrder: PERIDINIALES

Armoured, plated, free-living unicells, with symmetrical apical plates. Marine andfreshwater.

Includes: Glenodinium, Gyrodinium, PeridiniumOrder: PHYTODINIALES

Coccoid dinoflagellates with thick cell walls but lacking thecal plates. Manyepiphytic for part of life history. Some in plankton of humic fresh waters.

Includes: HemidiniumCLASS: AdinophyceaeOrder: PROROCENTRALES

Naked or cellulose-covered cells comprising two watchglass-shaped halves.Marine and freshwater species.

Includes: Exuviella, Prorocentrum

pigments, called phycobilins, are associated withthese membranes, where they are carried ingranular phycobilisomes. Life forms among theCyanobacteria have diversified from simple coc-coids and rods into loose mucilaginous colonies,called coenobia, into filamentous and to pseu-dotissued forms. Four main evolutionary lines

are recognised, three of which (the chroococ-calean, the oscillatorialean and the nostocalean;the stigonematalean line is the exception) havemajor planktic representatives that have diversi-fied greatly among marine and freshwater sys-tems. The most ancient group of the surviv-ing groups of photosynthetic organisms is, in

THE DIVERSIFICATION OF PHYTOPLANKTON 11

terms of individuals, the most abundant on theplanet.

Links to eukaryotic protists, plants and ani-mals from the Cyanobacteria had been sup-posed explicitly and sought implicitly. The dis-covery of a prokaryote containing chlorophyll aand b but lacking phycobilins, thus resemblingthe pigmentation of green plants, seemed tofit the bill (Lewin, 1981). Prochloron, a symbiontof salps, is not itself planktic but is recover-able in collections of marine plankton. The firstdescription of Prochlorothrix from the freshwa-ter phytoplankton in the Netherlands (Burger-Wiersma et al., 1989) helped to consolidate theimpression of an evolutionary missing link ofchlorophyll-a- and -b-containing bacteria. Thencame another remarkable finding: the mostabundant picoplankter in the low-latitude oceanwas not a Synechococcus, as had been thitherto sup-posed, but another oxyphototrophic prokaryotecontaining divinyl chlorophyll-a and -b pigmentsbut no bilins (Chisholm et al., 1988, 1992); it wasnamed Prochlorococcus. The elucidation of a bio-spheric role of a previously unrecognised organ-ism is achievement enough by itself (Pinevichet al., 2000); for the organisms apparently tooccupy this transitional position in the evolu-tion of plant life doubles the sense of scientificsatisfaction. Nevertheless, subsequent investiga-tions of the phylogenetic relationships of thenewly defined Prochlorobacteria, using immuno-logical and molecular techniques, failed to groupProchlorococcus with the other Prochlorales or evento separate it distinctly from Synechococcus (Mooreet al., 1998; Urbach et al., 1998). The present viewis that it is expedient to regard the Prochloralesas aberrent Cyanobacteria (Lewin, 2002).

The common root of all eukaryotic algae andhigher plants is now understood to be basedupon original primary endosymbioses involv-ing early eukaryote protistans and Cyanobacteria(Margulis, 1970, 1981). As more is learned aboutthe genomes and gene sequences of microorgan-isms, so the role of lateral gene transfers inshaping them is increasingly appreciated (Doolit-tle et al., 2003). For instance, in terms of ultra-structure, the similarity of 16S rRNA sequences,several common genes and the identical pho-tosynthetic proteins, all point to cyanobacterial

origin of eukaruote plastids (Bhattacharya andMedlin, 1998; Douglas and Raven, 2003). Prag-matically, we may judge this to have been ahighly successful combination. There may wellhave been others of which nothing is known,apart from the small group of glaucophytes thatcarry cyanelles rather than plastids. The cyanellesare supposed to be an evolutionary interme-diate between cyanobacterial cells and chloro-plasts (admittedly, much closer to the latter).Neither cyanelles nor plastids can grow inde-pendently of the eukaryote host and they areapportioned among daughters when the host celldivides. There is no evidence that the handfulof genera ascribed to this phylum are closelyrelated to each other, so it may well be an arti-ficial grouping. Cyanophora is known from theplankton of shallow, productive calcareous lakes(Whitton in John et al., 2002).

Molecular investigation has revealed that theseemingly disparate algal phyla conform to oneor other of two main lineages. The green lineof eukaryotes with endosymbiotic Cyanobacteriareflects the development of the chlorophyte andeuglenophyte phyla and to the important off-shoots to the bryophytes and the vascular plantphyla. The red line, with its secondary and eventertiary endosymbioses, embraces the evolutionof the rhodophytes, the chrysophytes and thehaptophytes, is of equal or perhaps greater fas-cination to the plankton ecologist interested indiversity.

A key distinguishing feature of the algae ofthe green line is the inclusion of chlorophyllb among the photosynthetic pigments and, typ-ically, the accumulation of glucose polymers(such as starch, paramylon) as the main prod-uct of carbon assimilation. The subdivision ofthe green algae between the prasinophyte andthe chlorophyte phyla reflects the evolutionarydevelopment and anatomic diversification withinthe line, although both are believed to havea long history on the planet (1.5 Ga). Bothare also well represented by modern genera, inwater generally and in the freshwater phyto-plankton in particular. Of the modern prasino-phyte orders, the Pedinomonadales, the Chloro-dendrales and the Pyramimonadales each havesignificant planktic representation, in the sense

12 PHYTOPLANKTON

of producing populations of common occurrenceand forming blooms on occasions. Several mod-ern chlorophyte orders (including Oedogoniales,Chaetophorales, Cladophorales, Coleochaetales,Prasiolales, Charales, Ulvales a.o.) are withoutmodern planktic representation. In contrast,there are large numbers of volvocalean, chloro-coccalean and zygnematalean species in lakesand ponds and the Tetrasporales and Ulotrichalesare also well represented. These show a very widespan of cell size and organisation, with flagel-lated and non-motile cells, unicells and filamen-tous or ball-like coenobia, with varying degrees ofmucilaginous investment and of varying consis-tency. The highest level of colonial developmentis arguably in Volvox, in which hundreds of net-worked biflagellate cells are coordinated to bringabout the controlled movement of the whole.Colonies also reproduce by the budding off andrelease of near-fully formed daughter colonies.The desmid members of the Zygnematales areamongst the best-studied green plankters. Mostlyunicellular, the often elaborate and beautifularchitecture of the semi-cells invite the gaze andcuriosity of the microscopist.

The euglenoids are unicellular flagellates.A majority of the 800 or so known speciesare colourless heterotrophs or phagotrophs andare placed by zoologists in the protist orderEuglenida. Molecular investigations reveal themto be a single, if disparate group, some of whichacquired the phototrophic capability throughsecondary symbioses. It appears that even thephototrophic euglenoids are capable of absorb-ing and assimilating particular simple organicsolutes. Many of the extant species are associ-ated with organically rich habitats (ponds andlagoons, lake margins, sediments).

The red line of eukaryotic evolution is basedon rhodophyte plastids that contain phycobilinsand chlorophyll a, and whose single thylakoidslie separately and regularly spaced in the plastidstroma (see, e.g., Kirk, 1994). The modern phy-lum Rhodophyta is well represented in marine(especially; mainly as red seaweeds) and fresh-water habitats but no modern or extinct plank-tic forms are known. However, among the inter-esting derivative groups that are believed toowe to secondary endosymbioses of rhodophyte

cells, there is a striking variety of plankticforms.

Closest to the ancestral root are the cryp-tophytes. These contain chlorophyll c2, as wellas chlorophyll a and phycobilins, in plastid thy-lakoids that are usually paired. Living cells aregenerally green but with characteristic, species-specific tendencies to be bluish, reddish orolive-tinged. The modern planktic representativesare exclusively unicellular; they remain poorlyknown, partly because thay are not easy toidentify by conventional means. However, about100 species each have been named for marineand fresh waters, where, collectively, they occurwidely in terms of latitude, trophic state andseason.

Next comes the small group of single-celled flagellates which, despite showing similar-ities with the cryptophytes, dinoflagellates andeuglenophytes, are presently distinguished in thephylum Raphidophyta. One genus, Gonyostomum,is cosmopolitan and is found, sometimes in abun-dance, in acidic, humic lakes. The green colourimparted to these algae by chlorophyll a is, tosome extent, masked by a xanthophyll (in thiscase, diatoxanthin) to yield the rather yellowishpigmentation. This statement applies even moreto the yellow-green algae making up the phylaXanthophyta and Eustigmatophyta. The xantho-phytes are varied in form and habit with anumber of familiar unicellular non-flagellate orbiflagellate genera in the freshwater plankton, aswell as the filamentous Tribonema of hard-waterlakes. The eustigmatophytes are unicellular coc-coid flagellates of uncertain affinities that taketheir name from the prominent orange eye-spots.

The golden algae (Chrysophyta) represent afurther recombination along the red line, giv-ing rise to a diverse selection of modern unicel-lular, colonial or filamentous algae. With a dis-tinctive blend of chlorophyll a, c1 and c2, and themajor presence of the xanthophyll fucoxanthin,the chrysophytes are presumed to be close tothe Phaeophyta, which includes all the macro-phytic brown seaweeds but no planktic vege-tative forms. Most of the chrysophytes have,in contrast, remained microphytic, with numer-ous planktic genera. A majority of these comefrom fresh water, where they are traditionally

THE DIVERSIFICATION OF PHYTOPLANKTON 13

supposed to indicate low nutrient status and pro-ductivity (but see Section 3.4.3: they may simplybe unable to use carbon sources other than car-bon dioxide). Mostly unicellular or coenobial flag-ellates, many species are enclosed in smoothprotective loricae, or they may be beset withnumerous delicate siliceous scales. The group hasbeen subject to considerable taxonomic revisionand reinterpretation of its phylogenies in recentyears. The choanoflagellates (formerly Craspedo-phyceae, Order Monosigales) are no longer con-sidered to be allied to the Chrysophytes.

The last three phyla named in Table 1.1,each conspicuously represented in both limneticand marine plankton indeed, they are themain pelagic eukaryotes in the oceans arealso remarkable in having relatively recent ori-gins, in the mesozoic period. The Bacillariophyta(the diatoms) is a highly distinctive phylum ofsingle cells, filaments and coenobia. The char-acteristics are the possession of golden-brownplastids containing the chlorophylls a, c1 andc2 and the accessory pigment fucoxanthin, andthe well-known presence of a siliceous frustuleor exoskeleton. Generally, the latter takes theform of a sort of lidded glass box, with one oftwo valves fitting in to the other, and bound byone or more girdle bands. The valves are oftenpatterned with grooves, perforations and callosi-ties in ways that greatly facilitate identification.Species are ascribed to one or other of the twomain diatom classes. In the Biddulphiales, orcentric diatoms, the valves are usually cylindri-cal, making a frustule resembling a traditionalpill box; in the Bacillariales, or pennate diatoms,the valves are elongate but the girdles are short,having the appearance of the halves of a datebox. While much is known and has been writ-ten on their morphology and evolution (see, forinstance, Round et al., 1990), the origin of thesiliceous frustule remains obscure.

The Haptophyta are typically unicellular goldor yellow-brown algae, though having amoeboid,coccoid or palmelloid stages in some cases. Thepigment blend of chlorophylls a, c1 and c2,with accessory fucoxanthin, resembles that ofother gold-brown phyla. The haptophytes are dis-tinguished by the possession of a haptonema,located between the flagella. In some species it

is a prominent thread, as long as the cell; in oth-ers it is smaller or even vestigial but, in mostinstances, can be bent or coiled. Most of theknown extant haptophyte species are marine;some genera, such as Chrysochromulina, are rep-resented by species that are relatively frequentmembers of the plankton of continental shelvesand of mesotrophic lakes. Phaeocystis is anotherhaptophyte common in enriched coastal waters,where it may impart a visible yellow-green colourto the water at times, and give a notoriously slimytexture to the water (Hardy, 1964).

The coccolithophorids are exclusively marinehaptophytes and among the most distinctivemicroorganisms of the sea. They have a charac-teristic surface covering of coccoliths flattened,often delicately fenestrated, scales impregnatedwith calcium carbonate. They fossilise particu-larly well and it is their accumulation whichmainly gave rise to the massive deposits of chalkthat gave its name to the Cretaceous (from Greekkreta, chalk) period, 12065 Ma BP. Modern coc-colithophorids still occur locally in sufficient pro-fusion to generate white water events. One ofthe best-studied of the modern coccolithophoridsis Emiliana.

The final group in this brief survey is thedinoflagellates. These are mostly unicellular,rarely colonial biflagellated cells; some are rel-atively large (up to 200 to 300 m across) andhave complex morphology. Pigmentation gener-ally, but not wholly, reflects a red-line ancestry,the complex plastids containing chlorophyll a,c1 and c2 and either fucoxanthin or peridininas accessory pigments, possibly testifying to ter-tiary endosymbioses (Delwiche, 2000). The groupshows an impressive degree of adaptive radia-tion, with naked gymnodinioid nanoplanktersthrough to large, migratory gonyaulacoid swim-mers armoured with sculpted plates and to deep-water shade forms with smooth cellulose wallssuch as Pyrocystis. Some genera are non-plankticand even pass part of the life cycle as epiphytes.Freshwater species of Ceratium and larger speciesof Peridinium are conspicuous in the planktonof certain types of lakes during summer strati-fication, while smaller species of Peridinium andother genera (e.g. Glenodinium) are associated withmixed water columns of shallow ponds.

14 PHYTOPLANKTON

Figure 1.1 Non-motileunicellular phytoplankters.(a) Synechococcus sp.; (b) Ankyrajudayi; (c) Stephanodiscus rotula;(d) Closterium cf. acutum. Scale bar,10 m. Original photomicrographsby Dr H. M. Canter-Lund,reproduced from Reynolds (1984a).

The relatively recent appearance of diatoms,coccolithophorids and dinoflagellates in thefossil record provides a clear illustration ofhow evolutionary diversification comes about.Although it cannot be certain that any of thesethree groups did not exist beforehand, thereis no doubt about their extraordinary rise dur-ing the Mesozoic. The trigger may well havebeen the massive extinctions towards the end ofthe Permian period about 250 Ma BP, when ahuge release of volcanic lava, ash and shroud-ing dust from what is now northern Siberiabrought about a world-wide cooling. The trendwas quickly reversed by accumulating atmo-spheric carbon dioxide and a period of severeglobal warming (which, with positive feedbackof methane mobilisation from marine sediments,raised ambient temperatures by as much as

1011 C). Life on Earth suffered a severe set-back, perhaps as close as it has ever cometo total eradication. In a period of less than0.1 Ma, many species fell extinct and the sur-vivors were severely curtailed. As the planetcooled over the next 20 or so million years,the rump biota, on land as in water, were ableto expand and radiate into habitats and nichesthat were otherwise unoccupied (Falkowski,2002).

Dinoflagellate fossils are found in the earlyTriassic, the coccolithophorids from the late Tri-assic (around 180 Ma BP). Together with thediatoms, many new species appeared in the Juras-sic and Cretaceous periods. In the sea, these threegroups assumed a dominance over most otherforms, the picocyanobacteria excluded, whichpersists to the present day.

GENERAL FEATURES OF PHYTOPLANKTON 15

Figure 1.2 Planktic unicellularflagellates. (a) Two variants ofCeratium hirundinella; (b)overwintering cyst of Ceratiumhirundinella, with vegetative cell forcomparison; (c) empty case ofPeridinium willei to show exoskeletalplates and flagellar grooves; (d)Mallomonas caudata; (e) Plagioselmisnannoplanctica; (f) two cells ofCryptomonas ovata; (g) Phacuslongicauda; (h) Euglena sp.; (j)Trachelomonas hispida. Scale bar, 10m. Original photomicrographs byDr H. M. Canter-Lund, reproducedfrom Reynolds (1984a).

1.4 General features ofphytoplankton

Despite being drawn from a diverse range ofwhat appear to be distantly related phyloge-netic groups (Table 1.1), there are features thatphytoplankton share in common. In an earlierbook (Reynolds, 1984a), I suggested that thesefeatures reflected powerful convergent forces inevolution, implying that the adaptive require-ments for a planktic existence had risen inde-pendently within each of the major phyla repre-sented. This may have been a correct deduction,although there is no compelling evidence thatit is so. On the other hand, for small, unicellu-lar microorganisms to live freely in suspensionin water is an ancient trait, while the transitionto a full planktic existence is seen to be a rel-atively short step. It remains an open questionwhether the supposed endosymbiotic recombina-tions could have occurred in the plankton, or

whether they occurred among other precursorsthat subsequently established new lines of plank-tic invaders.

It is not a problem that can yet be answeredsatisfactorily. However, it does not detract fromthe fact that to function and survive in theplankton does require some specialised adapta-tions. It is worth emphasising again that just asphytoplankton comprises organisms other thanalgae, so not all algae (or even very many ofthem) are necessarily planktic. Moreover, neitherthe shortness of the supposed step to a plank-tic existence nor the generally low level of struc-tural complexity of planktic unicells and coeno-bia should deceive us that they are necessarilysimple organisms. Indeed, much of this bookdeals with the problems of life conducted in afluid environment, often in complete isolationfrom solid boundaries, and the often sophisti-cated means by which planktic organisms over-come them. Thus, in spite of the diversity of phy-logeny (Table 1.1), even a cursory considerationof the range of planktic algae (see Figs. 1.11.5)

16 PHYTOPLANKTON

Figure 1.3 Coenobialphytoplankters. Colonies of thediatoms (a) Asterionella formosa, (b)Fragilaria crotonensis and (d) Tabellariaflocculosa var. asterionelloides. Thefenestrated colony of thechlorophyte Pediastrum duplex isshown in (c). Scale bar, 10 m.Original photomicrographs by DrH. M. Canter-Lund, reproducedfrom Reynolds (1984a).

reveals a commensurate diversity of form, func-tion and adaptive strategies.

What features, then, are characteristic andcommon to phytoplankton, and how have theybeen selected? The overriding requirements ofany organism are to increase and multiply itskind and for a sufficient number of the progenyto survive for long enough to be able to investin the next generation. For the photoautotroph,this translates to being able to fix sufficient car-bon and build sufficient biomass to form thenext generation, before it is lost to consumersor to any of the several other potential fates thatawait it. For the photoautotroph living in water,the important advantages of archimedean sup-port and the temperature buffering afforded bythe high specific heat of water (for more, seeChapter 2) must be balanced against the diffi-cuties of absorbing sufficient nutriment fromoften very dilute solution (the subject of Chapter4) and of intercepting sufficient light energy tosustain photosynthetic carbon fixation in excess

of immediate respiratory needs (Chapter 3). How-ever, radiant energy of suitable wavelengths(photosynthetically active radiation, or PAR) is nei-ther universally or uniformly available in waterbut is sharply and hyperbolically attenuated withdepth, through its absorption by the water andscattering by particulate matter (to be discussedin Chapter 3). The consequence is that for agiven phytoplankter at anything more than afew meters in depth, there is likely to be a crit-ical depth (the compensation point) below whichnet photosynthetic accumulation is impossible.It follows that the survival of the phytoplankterdepends upon its ability to enter or remain inthe upper, insolated part of the water mass forat least part of its life.

This much is well understood and the pointhas been emphasised in many other texts. Thesehave also proffered the view that the essentialcharacteristic of a planktic photoautotroph is tominimise its rate of sinking. This might be liter-ally true if the water was static (in which case,

GENERAL FEATURES OF PHYTOPLANKTON 17

Figure 1.4 Filamentousphytoplankters. Filamentouscoenobia of the diatom Aulacoseirasubarctica (a, b; b also shows aspherical auxospore) and of theCyanobacteria (c) Gloeotrichiaechinulata, (d) Planktothrix mougeotii,(e) Limnothrix redekei (note polar gasvacuoles), (f) Aphanizomenonflos-aquae (with one akinete formedand another differentiating) andAnabaena flos-aquae (g) in India ink,to show the extent of mucilage, and(h) enlarged, to show twoheterocysts and one akinete. Scalebar, 10 m. Originalphotomicrographs by Dr H. M.Canter-Lund, reproduced fromReynolds (1984a).

neutral buoyancy would provide the only idealadaptation). However, natural water bodies arealmost never still. Movement is generated as aconsequence of the water being warmed or cool-ing, causing convection with vertical and hori-zontal displacements. It is enhanced or modifiedby gravitation, by wind stress on the water sur-face and by the inertia due to the Earths rotation(Coriolis force). Major flows are compensated byreturn currents at depth and by a wide spectrumof intermediate eddies of diminishing size andof progressively smaller scales of turbulent diffu-sivity, culminating in molecular viscosity (thesemotions are characterised in Chapter 2).

To a greater or lesser degree, these move-ments of the medium overwhelm the sinking tra-jectories of phytoplankton. The traditional viewof planktic adaptations as mechanisms to slowsinking rate needs to be adjusted. The essentialrequirement of phytoplankton is to maximise theopportunities for suspension in the various partsof the eddy spectrum. In many instances, theadaptations manifestly enhance the entrainabil-ity of planktic organisms by turbulent eddies.These include small size and low excess den-sity (i.e. organismic density is close to that ofwater, 1000 kg m3), which features do con-tribute to a slow rate of sinking. They also include

18 PHYTOPLANKTON

Figure 1.5 Colonialphytoplankters. Motile colonies of(a) Volvox aureus, with (b) detail ofcells, (c) Eudorina elegans, (d)Uroglena sp. and (e) Dinobryondivergens; and non-motile colonies,all mounted in India ink to show theextent of mucilage, of (f) Microcystisaeruginosa, (g) Pseudosphaerocystislacustris and (h) Dictyosphaeriumpulchellum. Scale bar, 10 m.Original photomicrographs by DrH. M. Canter-Lund, reproducedfrom Reynolds (1984a).

mechanisms for increasing frictional resistancewith the water, independently of size and dens-ity. At the same time, other phytoplankters showadaptations that favour disentrainment, at leastfrom weak turbulence, coupled with relativelylarge size (often achieved by colony formation),streamlining and an ability to propel themselvesrapidly through water. Such organisms exploit adifferent part of the eddy spectrum from the firstgroup. The principle extends to the larger organ-

isms of the nekton, cephalopods, fish, reptilesand mammals which are able to direct theirown movements to overcome a still broader rangeof the pelagic eddy spectrum.

All these aspects of turbulent entrainmentand disentrainment are explored more deeplyand more empirically in Chapter 2. For themoment, it is important to understand how theyimpinge upon phytoplankton morphology in ageneral sense.

GENERAL FEATURES OF PHYTOPLANKTON 19

1.4.1 Size and shapeApart from the issue of suspension, there isa further set of constraints that resists largesize among phytoplankters. Autotrophy implies arequirement for inorganic nutrients that must beabsorbed from the surrounding medium. Theseare generally so dilute and so much much lessconcentrated than they have to be inside theplankters cell that uptake is generally against avery steep concentration gradient that requiresthe expenditure of energy to counter it. Onceinside the cell, the nutrient must be translo-cated to the site of its deployment, invoking dif-fusion and transport along internal molecularpathways. Together, these twin constraints placea high premium on short internal distances:cells that are absolutely small or, otherwise,have one or two linear dimensions truncated (sothat cells are flattened or are slender) benefitfrom this adaptation. Conversely, simply increas-ing the diameter (d) of a spherical cell is toincrease the constraint for, though the surfacearea increases in proportion to d2, the volumeincreases with d3. However, distortion from thespherical form, together with surface convolu-tion, provides a way of increasing surface incloser proportion to increasing volume, so thatthe latter is enclosed by relatively more sur-face than the geometrical minimum requiredto bound the same volume (a sphere). In thisrespect, the adaptive requirements for maximis-ing entrainability and for enhancing the assim-ilation of nutrients taken up across the surfacecoincide.

It is worth adding, however, that nutrientuptake from the dilute solution is enhancedif the medium flows over the cell surface, dis-placing that which may have already becomedepleted. Movement of the cell relative to theadjacent water achieves the similar effect, withmeasurable benefit to uptake rate (Pasciak andGavis, 1974; but see discussion in Section 4.2.1).It may be hypothesised that it is advantageousfor the plankter not to achieve isopycnic suspen-sion in the water but to retain an ability to sinkor float relative to the immediate surroundings,regardless of the rate and direction of travel ofthe latter, just to improve the sequestration ofnutrients.

These traits are represented and sometimesblended in the morphological adaptations of spe-cific plankters. They can be best illustrated bythe plankters themselves and by examining howthey influence their lives and ecologies. The wideranges of form, size, volume and surface areaare illustrated by the data for freshwater plank-ton presented in Table 1.2. The list is an edited,simplified and updated version of a similar tablein Reynolds (1984a) which drew on the authorsown measurements but quoted from other com-pilations (Pavoni, 1963; Nalewajko, 1966; Besch etal., 1972; Bellinger, 1974; Findenegg, Nauwerckin Vollenweider, 1974; Willn, 1976; Bailey-Watts,1978; Trevisan, 1978). The sizes are not preciseand are often variable within an order of mag-nitude. However, the listing spans nearly eightorders, from the smallest cyanobacterial unicellsof 1 m3 or less, the composite structures ofmulticellular coenobia and filaments with vol-umes ranging between 103 and 105 m3, throughto units of >106 m3 in which cells are embeddedwithin a mucilaginous matrix. Indeed, the list isconservative in so far as colonies of Microcystis of>1 mm in diameter have been observed in nature(authors observations; i.e. up to 109 m3 in vol-ume). Because all phytoplankters are small inhuman terms, requiring good microscopes to seethem, it is not always appreciated that the nineor more orders of magnitude over which theirsizes range is comparable to that spanning foresttrees to the herbs growing at their bases. Like theexample, the biologies and ecologies of the indi-vidual organisms vary considerably through thespectrum of sizes.

1.4.2 Regulating surface-to-volume ratioDwelling on the issue of size and shape, we willfind, as already hinted above, that a good dealof plankton physiology is correlated to the ratioof the surface area of a unit (s) to its volume(v). Unit in this context refers to the live habitof the plankter: where the vegetative form isunicellular (exemplified by the species listed inTable 1.2A), it is only the single cell that interactswith its environment and is, plainly, synonymouswith the unit. If cells are joined together tocomprise a larger single structure, for whateveradvantage, then the individual cells are no longer

20 PHYTOPLANKTON

Table 1.2 Nominal mean maximum linear dimensions (MLD), approximate volumes (v) andsurface areas (s) of some freshwater phytoplankton

MLD v s s/vSpecies Shape (m) (m3) (m2) (m1)

(A) UnicellsSynechoccoccus ell 4 18

(120)35 1.94

Ankyra judayi bicon 16 24(367)

60 2.50

Monoraphidium griffithsii cyl 35 30 110 3.67Chlorella pyrenoidosa sph 4 33

(840)50 1.52

Kephyrion littorale sph 5 65 78 1.20Plagioselmis

nannoplancticaell 11 72

(39134)108 1.50

Chrysochromulina parva cyl 6 85 113 1.33Monodus sp. ell 8 105 113 1.09Chromulina sp. ell 15 440 315 0.716Chrysococcus sp. sph 10 520 315 0.596Stephanodiscus

hantzschiicyl 11 600

(1801 200)404 0.673

Cyclotella praeterissima cyl 10 760(540980)

460 0.605

Cyclotella meneghiniana cyl 15 1 600 780 0.488Cryptomonas ovata ell 21 2710

(1 9503 750)1 030 0.381

Mallomonas caudata ell 40 4 200(3 42010 000)

3 490 0.831

Closterium aciculare bicon 360 4 520 4 550 1.01Stephanodiscus rotula cyl 26 5 930

(2 22018 870)1 980 0.334

Cosmarium depressum (a) 24 7 780(40030 000)

2 770 0.356

Synedra ulna bicon 110 7 900 4 100 0.519Staurastrum pingue (b) 90 9 450

(4 92016 020)6 150 0.651

Ceratium hirundinella (c) 201 43 740(19 08062 670)

9 600 0.219

Peridinium cinctum ell 55 65 500(33 50073 100)

7 070 0.108

(B) CoenobiaDictyosphaerium

pulchellum (40 cells)(d ) 40 900 1 540 1.71

Scenedesmusquadricauda (4 cells)

(e) 80 1 000 908 0.908

Asterionella formosa(8 cells)

(f ) 130 5 160(4 4306 000)

6 690 1.30

(cont.)

GENERAL FEATURES OF PHYTOPLANKTON 21

Table 1.2 (cont.)

MLD v s s/vSpecies Shape (m) (m3) (m2) (m1)

Fragilaria crotonensis(10 cells)

(g) 70 6 230(4 9707 490)

9 190 1.48

Dinobryon divergens(10 cells)

(h) 145 7 000(6 0008 500)

5 350 0.764

Tabellaria flocculosa var.asterionelloides(8 cells)

(f ) 96 13 800(6 52013 600)

9 800 0.710

Pediastrum boryanum(32 cells)

( j ) 100 16 000 18 200 1.14

(C) FilamentsAulacoseira subarctica

(10 cells)cyl (k) 240 5 930

(4 7407 310)4 350 0.734

Planktothrix mougeotii(1 mm length)

cyl (k) 1000 46 600 24 300 0.521

Anabaena circinalis (m) 60 2 040 2 110 1.03(20 cells) (n) 75 29 000 6 200 0.214

Aphanizomenon (p) 125 610 990 1.62flos-aquae (50 cells) (q) 125 15 400 5 200 0.338

(D) Mucilaginous coloniesCoenochloris fottii

(cells 801200 m3)sph 46 51 103 6.65 103 0.13

Eudorina unicocca(cells 1201200 m3)

sph 130 1.15 106 53.1 103 0.046

Uroglena lindii(cells 100 m3)

sph 160 2.2 106 81 103 0.037

Microcystis aeruginosa(cells 30100 m3)

sph 200 4.2 106 126 103 0.030

Volvox globator sph (r) 450 47.7 106 636 103 0.013(cells 60 m3) (s) 450 6.4 106 636 103 0.099

Notes: The volumes and surface areas are necessarily approximate. The values cited are those adoptedand presented in Reynolds (1984a); some later additions taken from Reynolds (1993a), mostly basedon his own measurements. The volumes given in brackets cover the ranges quoted elsewhere in theliterature (see text). Note that the volumes and surface areas are calculated by analogy to the nearestgeometrical shape. Surface sculpturing is mostly ignored. Shapes considered include: sph (for a sphere),cyl (cylinder), ell (ellipsoid), bicon (two cones fused at their bases, area of contact ignored from surfacearea calculation). Other adjustments noted as follows:a Cell visualised as two adjacent ellipsoids, area of contact ignored.b Cell visualised as two prisms and six cuboidal arms, area of contact ignored.c Cell visualised as two frusta on elliptical bases, two cylindrical (apical) and two conical (lateral) horns.d Coenobium envisaged as 40 contiguous spheres, area of contact ignored.e Coenobium envisaged as four adjacent cuboids, volume of spines ignoredf Coenobium envisaged as eight cuboids, area of contact ignored.

22 PHYTOPLANKTON

Notes to Table 1.2 (cont.)g Each cell visualised as four trapezoids; area of contact between cells ignored.h Coenobium envisaged as a seies of cones, area of contact ignoredj Coenobium envisaged as a discus-shaped sphaeroid.k Coenobium envisaged as a chain of cylinders, area of contact between cells ignored.l Coenobium envisaged as a single cylinder, terminal taper ignored.m Filament visualised as a chain of spheres, area of contact between them ignoredn Filament visualised as it appears in life, enveloped in mucilage, turned into a complete doughnut ring,with a cross-sectional diameter of 21 m.p Filament visualised as a chain of ovoids, area of contact between them ignored.q For the typical raft habit of this plankter, a bundle of filaments is envisaged, having an overall lengthof 125 m and a diameter of 12.5 m.r The volume calculation is based on the external dimensions.s In fact the cells in the vegetative stage are located exclusively on the wall of a hollow sphere. Thissecond volume calculation supposes an average wall thickness of 10 m and subtracts the hollow volume.

independent but rather constitute a multicellu-lar unit whose behaviour and experienced envi-ronment is simultaneously shared by all the oth-ers in the unit. Such larger structures may deploycells either in a plate- or ball-like coenobium (exem-plified by the species listed in Table 1.2B) or, end-to-end, to make a uniseriate filament (Table 1.2C).Generally, added complexity brings increased sizebut, as vol