ICES Zooplankton Methodology ManualThis Page Intentionally Left BlankICES Zooplankton Methodology ManualEdited byRoger HarrisPlymouth Marine LaboratoryProspect PlacePlymouth PL1 3DH, UKPeter WiebeWoods Hole Oceanographic InstitutionWoods HoleMA02543, USAJu rgen LenzInstitut fu r Meereskunde an der Universita t KielDu sternbrooker Weg 20Kiel D-24105, GermanyHein Rune SkjoldalInstitute of Marine ResearchPOBox 1870NordnesBergen N-5024, NorwayMark HuntleyHawaii Natural Energy InstituteSchool of Ocean and Earth Science and TechnologyUniversity of Hawaii at ManoaHonoluluHawaii 96822, USASan Diego San Francisco New York BostonLondon Sydney TokyoThis book is printed on acid-free paper.Copyright #2000 by ACADEMIC PRESSAll Rights Reserved.No part of this publication may be reproduced or transmitted in any form or by anymeans, electronic or mechanical, including photocopying, recording, or anyinformation storage and retrieval system, without permission in writing from thepublisher.Academic PressA Harcourt Science and Technology CompanyHarcourt Place, 32 Jamestown Road, London NW1 7BY, UKhttp://www.academicpress.comAcademic Press525 B Street, Suite 1900, San Diego, California 92101-4495, USAhttp://www.academicpress.comISBN 0-12-327645-4A catalogue for this book is available from the British LibraryTypeset by Paston PrePress Ltd, Beccles, SuolkPrinted in Great Britain by MPG Books Ltd, Bodmin, Cornwall00 01 02 03 04 05 MP 9 8 7 6 5 4 3 2 1CONTENTSList of Contributors xviiPreface xix1 Introduction 11.1 Introduction 11.2 General denitions 11.3 Size classication 31.4 Main systematic groups 51.5 Species diversity 61.6 Ecological position 81.7 Distribution pattern 101.8 Growth and metabolism 101.9 Reproduction and development 121.10 Standing stock and production 121.11 Conclusion 131.12 References 302 Sampling and experimental design 332.1 Introduction 332.2 Conceptual issues 34Increased emphasis on species dynamics 34Integration of disciplines: zooplankton, between physics and sh 35Integration of scales: from climatic to turbulent 36Integration of approaches: from theory to eld 37Integration of pattern and process 38Integration of technologies and methods 392.3 Design of oceanographic cruises and surveys 40Survey design considerations 40Survey design types 41Systematic design 41Random design 42Stratied random design 42Preferential design 42Other design types 42Sampling in ow elds 43Examples of eld programs 442.4 References 493 Collecting zooplankton 553.1 Introduction 553.2 A survey of sampling devices 57Pumps and traps 57Nets and serial samplers 58Simple net samplers 58Multiple sample instruments 58Multiple net samplers 623.3 Factors inuencing mesozooplankton samples 67Extrusion of zooplankton from nets 67Clogging of net mesh 70Avoidance 70Eect of ambient light 72Mesh and frame color 723.4 Handling towed samplers 723.5 Care of towing cables 743.6 Handling samples and sample preservation 743.7 Collection of live zooplankton for experimental studies 76Copepods 763.8 Other zooplankton instruments used in conjunction with nets 77Optical plankton counter 773.9 References 784 Biomass and abundance 834.1 Introduction 834.2 Shipboard sample treatment 854.3 Biovolume and biomass determinations (W. Hagen) 87Volumetric methods 88Settling volume 88Displacement volume 89Gravimetric methods 90Wet mass, fresh mass and live mass 90Dry mass 91Ash-free dry mass 94Biochemical methods 94Sample preparation 97Elemental analysis 97Organic carbon (and hydrogen) 101Organic nitrogen 103Organic phosphorus 105Organic compounds 107Proteins 107Lipids (W. Hagen) 113Carbohydrates 119Energy content 122Adenosine triphosphate ATP 131Conversion factors and equations 1394.4 Abundance and species identication 1474.5 Analysis of community structure (H. Fock) 154Estimation of species numbers 155Diversity and similarity indices 158Classication and ordination: the detection of groups 164Multivariate classication techniques 164vi CONTENTSRecurrent group analysis 166Matching species and samples: indicator species analysis 168Analysis of spatial and temporal formations 169Examination of processes within communities by network analysis 1734.6 Acknowledgment 1744.7 References 1745 Sampling, preservation, enumeration and biomass of marineprotozooplankton 1935.1 Introduction 1935.2 Collection methods 196Nano- and microzooplankton 196Planktonic sarcodines 1975.3 Preservation and enumeration 201Nanozooplankton 201Preservation 201Nanozooplankton enumeration 202Microzooplankton 203Microzooplankton preservation 203Microzooplankton enumeration 204Planktonic sarcodines 205Larger planktonic sarcodine preservation 205Larger planktonic sarcodine enumeration 2065.4 Determination of biomass: conversion factors 206Nanozooplankton 206Microzooplankton 207Planktonic sarcodines 2085.5 Standard protocols 210Collection of nano- and microzooplankton 210Preservation of nanozooplankton 210Staining and enumeration of nanozooplankton 210Preservation of microzooplankton 211Enumeration of microzooplankton 2125.6 Acknowledgments 2125.7 References 2126 Acoustical methods 2236.1 Introduction 2236.2 General discussion of principles, instruments, techniques, andcomparative approaches 223Review 223Background 223History 224Basic principles 224Active sonar equation 224Target strength models 226Sources of variability 231Measurement 231Modeling 232CONTENTS viiGeneric instruments 232Echo sounder 232Sonar 233Acoustic Doppler current proler (ADCP) 233Echo integrator 233Post-processing system 233Methods of data processing and analysis 234Echogram 234Echo integration 234Target strength determination 235Post-processing and data analysis 237Comparisons 238Identication 238Choosing an acoustic instrument 239Single-animal methods 239Multiple-animal methods 240Parameter ranges for scientic echo sounders 2406.3 Measurement protocols, model computations, and examples 241Calibration 241Test measurements 241Standard-target method 241Beam pattern measurement 242Elements of echo abundance surveying 243Equipment 243Signal processing 244Equipment use 244Medium 244Scatterer identication 244Survey planning 244Interpretation 244Density measurement 244Interpolation 244Abundance estimation 245System deployment 245Evaluation of sonar performance 245Exemplary model computations 248Echo abundance surveying of Antarctic krill 250Target strength determination by caged-animal measurement:Antarctic krill 251Monitoring zooplankton with a xed acoustic system 251Acoustic estimates of size distribution using a multi-frequency system 2526.4 Acknowledgments 2536.5 References 2537 Optical methods 2597.1 Introduction 2597.2 General discussion of principles, techniques, and comparativeapproaches 260Review 260viii CONTENTSBasic principles 261Light phenomena 261Illumination 262Water as an optical medium 263Light detection 264Magnication and resolution 264Sources of variability 265Instrument eects 265Water medium 265Animal-dependent eects 266Classes of light microscopy 266Imaging 266Bright-eld microscopy 267Contrast techniques 267Fluorescence microscopy 270Quantication 272Techniques 272Silhouette photography 272Optical plankton counting 273Video plankton recording 275Comparisons 281Identication 282Imaging versus quantication 283Venue and deployment 283Operating ranges of two systems 2837.3 Measurement protocols, model computations, and examples 283Silhouette photography in the laboratory 283Procedures 284Further processing of the lm 286Optical plankton counter 286Calibration including comparisons 286Limitations 288Operating scenario 288Applications 288Video plankton recorder 289Calibration including comparisons 289Limitations 290Operating scenario 290Applications 2917.4 Acknowledgments 2917.5 References 2918 Feeding 2978.1 Introduction 2978.2 Feeding mechanisms of zooplankton 2978.3 Expression of zooplankton feeding rates and common conversionfactors 299Clearance rate (F) 299Ingestion rate (I) 301CONTENTS ixDaily ration (DR) 302Conversions between units of mass and energy 3038.4 Microzooplankton 303Methodological approaches 303Indirect methods to measure assemblage grazing 306Correlation of natural consumerprey cycles 306Extrapolation of laboratory rates to the eld 306The pigment budget 307Acid lysozyme assay 307Direct methods to measure per capita grazing rates 308Food tracers: inert particles 308Food tracers: prey cells 310Food tracers: radioisotopes 311Food vacuole contents 313Prey removal 314Direct methods to measure assemblage grazing rates 314Sea water dilution method 314Working procedures for the sea water dilution method 316Size fractionation methods 319Metabolic inhibitor method 3208.5 Meso- and macrozooplankton 320Empirical relationships 320Field investigation on gut uorescence 322Sampling 323Preparation for analysis 323Gut clearance coecient 323Sorting animals 325Extraction 326Pigment analysis 326Transformation to carbon 327Pigment destruction 327Working procedures for the gut uorescence method 328Equipment 328Supplies 328Procedure 328Measurement and calculations 330Comments and special precautions 330Gut contents of eld sampled consumers 330General procedures 331Special case: copepod mandibles in stomach contents 332Digestion 333Methods based on budgets of material or energy 335Growth 336Egestion 336Excretion 337Respiration 337Assimilation eciency 337Measurement of assimilation eciency: direct measurements 338Measurement of assimilation eciency: indirect calculation 338x CONTENTSMeasurement of assimilation eciency: ratio methods 339Non-homogeneous food material 339Food selectivity 339Sloppy feeding 340Losses from fecal material 340Absorbance of IT in the digestive tract 340Production of non-fecal material mixed with feces 340Ash-ratio method 341Chlorophyl-ratio method 341Silica-ratio method 342Radioisotope tracers 342Methodological comparisons 343Working procedures for laboratory experiments with isotopes 343Working procedures for eld experiments 344Food removal methods 344Bottle eects during incubations 345Sloppy feeding 346Estimates of community grazing rate 346Working procedures with food removal methods 350Collection of zooplankton 350The food source 351Experiments 351Sub-sampling 353Microscopic examination of sub-samples 354Feeding rate calculations 354Use of lm and video to study feeding behavior 355Biochemical indices 356Working procedures for measurement of digestive enzyme activity 358Amylase 358Trypsin 3588.6 Diculties with specic zooplankton groups 359Stomach contents from eld samples 359Laboratory experiments 3628.7 Omnivory 365A general method to estimate omnivory 365Collection of consumers 366Collection and handling of water 366Sample collection, processing and analysis 366Data analysis 367Gut uorescence and experimental egg production 367Gut uorescence and egestion rate 367A method to estimate the importance of copepod prey for predators 3678.8 Factors regulating feeding rate 368Abundance of food items 368Functional response. Model I 369Functional response. Model II 370Functional response. Modied model II 370Functional response. Model III 371Design of functional response experiments 371CONTENTS xiCalculation curve ts in functional response experiments 372Size of food items 373Turbulence 374Consumer body size 374Palatability/toxicity of food organisms 375Physical environmental factors 376Temperature 376Light 376Spatial constraints 3778.9 Predation behavioral models 3778.10 Concluding remarks 3788.11 Acknowledgments 3798.12 References 3809 The measurement of growth and reproductive rates 4019.1 Introduction: why measure growth and reproductive rates ofzooplankton? 401Factors controlling the dynamics of copepod populations 402Variability in the production of the prey eld for sh larvae 402The inuence of food availability on growth and egg laying rates,including the linkage between copepod spawning and primaryproduction cycles 402Evaluation of environmental impacts 402Estimation of secondary production 4039.2 Models of growth and fecundity 403Physiological or laboratory-derived budgetary models 404Temperature-dependent empirical model 405Global model of in-situ weight-specic growth 4069.3 Determination of egg production rate: broadcast spawning copepods 407The basic method 407Procedures: know your species 409Capture and handling 409Duration of incubation 410Incubation containers and density of females 410Temperature 413Light regime 414Food supply 414Statistical considerations 415Estimation of spawning frequency from preserved samples 416Egg viability 4169.4 Egg production rates of egg carrying copepods 418Egg ratio method 418Incubation method 4199.5 The determination of growth rate 420Estimation of growth rate from preserved samples anddemographic information 420Estimation of development time 420Estimation of mean weight 420Limitations and sources of error 421xii CONTENTSDirect measurement of growth rate 422The basic method 422Procedures 4239.6 Biochemical and radiochemical methods 425Ratio of biochemical quantities 425Hormones and growth factors 426Enzyme activities 427Radiochemical methods 433In vitro incorporation 433In vivo uptake 435In vivo injection 436In vivo ingestion 4369.7 Measurement of egg production rate of a marine planktoniccopepod (Calanus nmarchicus) 439Facilities 439Equipment and supplies 439Procedure 440Capture 440Sorting the catch 440Incubation 441Data analysis 4419.8 Direct determination of copepod molting and growth rates inthe eld 441Facilities and equipment 441Supplies 441Procedure 442`Articial cohort method' 442`Sorting method' 442Data analysis and interpretation 443Molting rates 443Growth rates 443Notes and comments 443Creation of articial cohorts: alternative techniques 443Changing the water 4449.9 Acknowledgments 4449.10 References 44410 Metabolism 455Review 45510.1 Oxygen consumption as an index of metabolism 455Conversion of oxygen consumption to carbon and caloric units 45810.2 Nitrogen and phosphorus metabolism 45810.3 Measuring metabolic rate on live zooplankton 460Technical problems 461Body size and temperature as bases of metabolic comparison 473Metabolic quotients 47610.4 Metabolic rate and enzymatic indices 479ETS activity 481Enzymes of intermediary metabolism 484CONTENTS xiiiPotential sources of error 48510.5 Concluding remarks 489Practice (T. Ikeda and J.J. Torres) 49010.6 Collection and handling of zooplankton 49010.7 Respiration 493Oxygen consumptionWinkler titration (T. Ikeda) 493Oxygen consumption electrodes (J.J. Torres) 499Enzymatic method electron transfer system (S. Herna ndez-Leo n) 506Enzymatic method lactate dehydrogenase and citrate synthase(J.J. Torres and S.P. Geiger) 51010.8 Excretion (T. Ikeda) 516Single end-point method 516Time-course method 517Ammonia and inorganic phosphate analysis 51710.9 References 52011 Methods for population genetic analysis of zooplankton 53311.1 Background 53311.2 Technical approaches to determining genetic diversity 534Allozymes 534Restriction fragment length polymorphisms of DNA 535DNA sequence analysis 536Oligonucleotide probe hybridization 537Allele-specic PCR 540Microsatellite DNA 540RAPDs 540New and emerging techniques 54211.3 Statistical approaches to assessing genetic diversity and structure 542Statistical measures of genetic diversity 543Statistical measures of genetic structure 545Statistical analysis of gene ow (dispersal) 547Computer methods and software sources 54711.4 Strategies for preservation of zooplankton samples forgenetic analysis 549Preservation and storage in ethanol 550Quick freezing in liquid nitrogen 550Formalin, glutaraldehyde, and other bad things 551Dehydration 551In situ molecular analysis 55111.5 General recommendations 55211.6 Measurement protocols 553Introduction 553Facilities and equipment 553General laboratory rules 554Procedures 554Sample preservation 554DNA purication 555PCR amplications 557Gel electrophoresis 559xiv CONTENTSGel purication of DNA 559Recipes and safety information 561Buers and frequently used solutions 561Safety information 56111.7 Further reading 56211.8 Acknowledgments 56311.9 References 56412 Modeling zooplankton dynamics 57112.1 Introduction 57112.2 Modeling approaches and techniques 572Steps of model building 572Choice of state and forcing variables 572Choice of model units 573Choice of mathematical functions to model the interactionsbetween variables 573Identication of parameters 573The mathematical description of the system 574Systems of equations 574Numerical methods 575Computer programing and languages 576Further reading 57612.3 Models of individual bioenergetics and life-history traits 577Individual bioenergetics 577Budget of individual zooplankton 577Ingestion rate 578Assimilation and egestion 585Excretion and respiration energetic costs 585Growth and egg production models 586Vital rates 589Developmental stage durations of crustacean zooplankton 590Mortality rates 591Inverse methods to estimate vital rates 592Evolutionary forces on the organism 592Further reading 59512.4 Population models 595Populations described by one variable 595Populations described by several variables structuredpopulation models 595Discrete-time dierence equation models and matrix models 596Continuous-time structured population models 600Stage-structured population models based on ODEs 602Delay dierential equation models 606Structured population models to estimate demographic parameters 606Stochasticity in structured population models 606Individual-based models of a population 606Building an IBM 607Object-oriented programing (OOP) 609Constraints in behavior 609CONTENTS xvModels of interactions between zooplanktonic populations 610Interaction model with two variables 610Population interactions using structured population models 611Further reading 61112.5 Models of zooplankton communities 612Zooplankton bulk models in ecosystem models 612The representation of herbivorous zooplankton in NPZ-typeecosystem models 612From a single grazer to several grazers 618Size-structured zooplanktonic community 620Size-structured ecosystem models 620Size spectrum theory 621Size- and stage-structured zooplankton populations inecosystem models 623Further reading 62312.6 Modeling spatial dynamics of zooplankton 624Modeling active behavior and counter-gradient search 624Modeling behavioral mechanisms, aggregation and schooling patches 625Modeling zooplankton behavior at the `micro-scale' 625Evolutionary modeling approaches for optimal spatial distributions 627Models of plankton patchiness generated by population dynamicsinteractions 633Grid-based models 634Coupling IBMs and spatially explicit models 635Passive particle trajectories from Lagrangian transport in modelcirculation elds 635Trajectories of actively swimming particles from Lagrangian transportin model circulation elds 637Spatial zooplankton dynamics with advection-diusion-reactionequations (ADRE) 638Modeling passive dispersion with ADREs 639Modeling active vertical swimming with ADREs 640Modeling the dispersion of a population in circulation modelswith ADREs 642Spatial distribution of zooplankton in ecosystem models coupledwith ADREs 643Further reading 64312.7 Acknowledgments 64312.8 References 644Index 669xvi CONTENTSCONTRIBUTORSA. Atkinson British Antarctic Survey, Natural Environment Research Council, HighCross, Madingley Road, Cambridge CB3 0ET, UKU. Ba mstedt Department of Fisheries and Marine Biology, University of Bergen, TheHigh Technology Centre, PO Box 7800, N-5020 Bergen, NorwayA. Bucklin Department of Zoology and Institute for the Study of Earth, Oceans, andSpace, 142 Morse Hall, University of New Hampshire, Durham, New Hampshire03824, USAF. Carlotti C.N.R.S., Universite Bordeaux 1, Laboratoire d'Oceanographie Biolog-ique, UMR 5805, 2 rue de Professeur Jolyet, F-33120 Arcachon, FranceD.A. Caron Department of Biological Sciences, University of Southern California,3616 Trousdale Parkway, AHF 309, Los Angeles, CA 90089-0371, USAS.H. Coombs Plymouth Marine Laboratory, Prospect Place, West Hoe, PlymouthPL1 3DH, UKJ. Dunn Marine Laboratory, PO Box 101, Victoria Road, Aberdeen, AB11 9DB, UKH. Fock Forschungsinstitut Senckenberg, Sektion Planktonforschung/Systemo kolo-gie, Geb. 111 DESY, Notkestrae 85, D-22607 Hamburg, GermanyK.G. Foote Institute of Marine Research, PO Box 1870, Nordnes, N-5817 Bergen,Norway (current: Woods Hole Oceanographic Institution, Woods Hole, MA 02543,USA)S.P. Geiger Department of Marine Science, University of South Florida, 140 SeventhAvenue South, St Petersburg, Florida 33701-5016, USAD.J. Giord Graduate School of Oceanography, University of Rhode Island, Narra-gansett, RI 02882-1197, USAJ. Giske Department of Fisheries and Marine Biology, University of Bergen,Hyteknologisenteret, N-5020 Bergen, NorwayW. Hagen Marine Zoologie (FB2), Universita t Bremen (NW2A), PF 330440, D-28334Bremen, GermanyS. Herna ndez-Leo n Facultad de Ciencias del Mar, Universidad de Las Palmas de GranCanaria, Campus Universitario de Tara, 35017 Las Palmas de GC, Canary Islands,SpainT. Ikeda Biological Oceanography Laboratory, Faculty of Fisheries, Hokkaido Uni-versity, Hakodate 041 JapanX. Irigoien Plymouth Marine Laboratory, Prospect Place, Plymouth PL1 3DH, UKJ. Lenz Institu t fur Meereskunde an der Universita t Kiel, Du sternbrooker Weg 20,D-24105 Kiel, GermanyC. Miller College of Oceanic and Atmospheric Sciences, Oregon State University,104 Ocean Administration Building, Corvallis, OR 97331-5503, USAL. Postel Institute of Baltic Sea Research, Seestr. 15, D-18119 Rostock-Warnemu nde,GermanyJ.C. Ro Department of Zoology, University of Guelph, Guelph, ON N1G 2W1,CanadaM. Roman Horn Point Environmental Laboratory, Box 775, Cambridge MD 21613,USAJ.A. Runge Fisheries and Oceans Canada, Institut Maurice-Lamontagne, 850 Routede la Mer, C.P. 1000, Mont Joli, QC, G5H 3Z4, CanadaD. Sameoto Department of Fisheries and Oceans, Bedford Institute of Oceanography,PO Box 1006, Dartmouth, NS B2Y 4A2, CanadaH.R. Skjoldal Institute of Marine Research, PO Box 1870, Nordnes, N-5024 Bergen,NorwayT.K. Stanton Woods Hole Oceanographic Institution, Woods Hole, MA 02543,USAJ.J. Torres Department of Marine Science, University of South Florida, 140 SeventhAvenue South, St. Petersburg, Florida 33701-5016, USAF. Werner Marine Science program, University of North Carolina, 12-7 Venable Hall,CB 3300, USAP.H. Wiebe Woods Hole Oceanographic Institution, Woods Hole, MA 02543, USAxviii CONTRIBUTORSPREFACEZooplankton are the diverse, delicate and often very beautiful, assemblage of animalsthat drift the waters of the world's oceans. These microscopic organisms play a key rolein the pelagic food web by controlling phytoplankton production and shaping pelagicecosystems. In addition, because of their critical role as a food source for larval andjuvenile sh, the dynamics of zooplankton populations, their reproductive cycles,growth, reproduction and survival rates are all important factors inuencing recruitmentto sh stocks. It is this latter role which has made zooplankton ecology of particularinterest to ICES.The International Council for the Exploration of the Sea, ICES, is the oldestintergovernmental organization in the world concerned with marine and sheriesscience. Since its establishment in Copenhagen in 1902, ICES has been a leadingscientic forum for the exchange of information and ideas on the sea and its livingresources, and for the promotion and coordination of marine research by scientistswithin its member countries. Each year, ICES holds more than 100 meetings of itsvarious working groups, study groups, workshops and committees.Membership has increased from the original eight countries in 1902 to the present 19countries which come from both sides of the Atlantic and include all European Coastalstates except the Mediterranean countries eastward of, and including, Italy. ICESestablished a Study Group on Zooplankton Production in 1992 chaired by Hein RuneSkjoldal, of the Institute of Marine Research, Bergen, Norway. The Study Group weregiven as terms of reference to:(a) review existing methods for measuring biomass and production processes;(b) make proposals for improvement and standardization of methods, and prepare amethodological manual;(c) consider the need for laboratory and seagoing workshops to intercalibrate experi-mental methods and evaluate new technology.The Study Group has met eight times, in March 1992 in Bergen; in March 1993 in LasPalmas; in March 1994 in Plymouth; in June 1995 in Woods Hole; in March 1996 inBergen; in March 1997 in Kiel, May 1998 in Santander, and May 1999 in Reykjavik. In1997 Roger Harris of the Plymouth Marine Laboratory, United Kingdom, assumed thechairmanship.The Study Group decided at the rst meeting to produce a Zooplankton MethodologyManual recognizing the need for improvements and standardization in methods forstudying this important and challenging group of organisms. To assist in the review ofmethods and to provide input to the issue of standardization and improvement ofmethods, three special workshops were convened. The rst was a seagoing workshoponboard RV Johan Hjort and RV A.V. Humboldt on zooplankton sampling methods(June 1993). The two others were laboratory workshops at the University of Bergen, onproduction methods using the copepods Acartia tonsa (October 1993) and Calanusnmarchicus (April 1994). A fourth workshop was arranged by US GLOBEC in Hawaiiusing marine copepods (April 1994). Results from these workshops have been incorpo-rated by the Study Group in producing this Manual.ICES changed the status of the Study Group to a Working Group on ZooplanktonEcology (WGZE) in 1994. The Working Group has taken over the task of completingwork with the Manual.The Scope of the Zooplankton Methodology Manual is to provide an updated reviewof basic methodology used in studies of zooplankton including recommendations onimprovements, harmonization and standardization of methods. The chapters aim tomaintain a balance between being introductory and comprehensive. They provide anoverview of methods that are useful, for example to graduate students who are startingin a new eld. They emphasize the sources of error and the strengths and weaknesses ofmethods for various purposes and tasks. It has not been possible, however, to go intogreat detail for all methods, and reference to recent reviews and detailed descriptions ofmethods is used where possible and appropriate.Each chapter begins with a review of methods which in most cases is accompanied byrecommendations regarding choice and conduct of methods. These reviews consider thebackground and history of the methodology, the basic principles, sources of variability,equipment and procedures, comparative evaluation of alternative methods, generalrecommendations, and extensive literature references. Where possible detailed descrip-tions of standard protocols are included. The aim is to give practical instructions on howto carry out particular measurements and procedures. Equipment, procedures, dataanalysis and interpretation are described, where possible. These protocols either denestandard methods, or give examples of little-known methods. If many methods are used,or many instruments, guidance is given on the most highly recommended, or the mostoften used, or likely to be used. In some cases it proves dicult to propose an agreedstandard protocol. It is however, possible to provide guidelines that reduce thevariability in methods and contribute towards harmonization and standardization.The various chapters of the Manual have been reviewed by the ICES WGZE, and inaddition peer reviewers from outside this group have evaluated each chapter indepen-dently. Grateful thanks are due to these reviewers for their valuable contribution to theoverall project.Each chapter is authored by an expert, or group of experts, selected from bothmembers of the WGZE and other international specialists. The writing has beenorganized and co-ordinated by the main author assisted by co-authors. Chapter 1provides an introduction to zooplankton. Chapters 2, 3, 4 and 5 consider sampling andexperimental design, collecting zooplankton, techniques for assessing biomass andabundance, and the specialized methodology required for protozooplankton enumera-tion and biomass estimation. Chapters 6 and 7 describe new and emerging optical andacoustic techniques for estimating zooplankton biomass and abundance. In chapters 8, 9and 10, methods for measuring zooplankton rate processes are described; feeding,growth and reproduction, and metabolism. Chapter 11 gives a modern account ofmethods for population genetic analysis of zooplankton, and Chapter 12 a comprehen-sive treatment of modelling zooplankton dynamics.While striving to be a comprehensive treatment of modern methods in zooplanktonecology, it is inevitable that some topics have not been covered. In particular it was theoriginal intention to include chapters on methods for investigating zooplanktonbehavior, and for studying population dynamics. The former chapter was nevercommissioned, while the latter although originally written as part of the ICES Manualproject, was ultimately published as a separate scientic article; Aksnes et al. 1997.Estimation techniques used in studies of copepod population dynamics a review ofunderlying assumptions. Sarsia, 82:279298. This may still be referred to as beingxx PREFACEcomplementary to the work. The original concept of the Zooplankton MethodologyManual included a related CD-ROM to include data, graphics and video images,particularly relating to sampling methods, and deriving from the seagoing workshop.This is not included with the Manual, however the WGZE are still considering thepreparation and distribution of such a CD-ROM.The ICES WGZE has been encouraging and co-ordinating zooplankton monitoringactivities in the ICES area, and this Manual should contribute to these activities.Similarly, the development of major international initiatives with a particular focus onzooplankton, particularly the IGBP/SCOR/IOC co-sponsored Global Ocean EcosystemDynamics (GLOBEC) project, and the Living Marine Resources module of the GlobalOcean Observing System (GOOS-LMR) make the publication of this Manual particu-larly timely. While not formally adopted by either program, the ICES ZooplanktonMethodology Manual will contribute signicantly to the standardization of methodol-ogy that both GLOBEC and GOOS-LMR strongly endorse.The preparation of the Zooplankton Methodology Manual has by denition been ateam eort. The members of the WGZE and the Editors have lead in this, over the yearsof development. It is a great pleasure to acknowledge the enthusiasm, dedication andpatience of all the authors and co-authors during this process. I am particularly gratefulto Dr Sarah Staord, Clare Nehammer and Teresa Netzler of Academic Press who haveall worked with me during the editing and production of the Manual.Plymouth Roger HarrisDecember 1999PREFACE xxiThis Page Intentionally Left Blank1 IntroductionJ. Lenz1.1 INTRODUCTIONZooplankton occupies a key position in the pelagic food web as it transfers theorganic energy produced by unicellular algae through photosynthesis to higher trophiclevels such as pelagic sh stocks exploitable by man. The availability of zooplankton ofthe right size and at the right place and time during the rst feeding period of sh larvaeconstitutes the famous match/mismatch hypothesis (Cushing 1990). Apart from pre-dation, it is regarded as the most important environmental factor controlling the yearclass strength of a large number of commercial sh stocks known to be subject to stronguctuations. Zooplankton grazing also largely determines the amount and compositionof vertical particle ux. This not only fuels the benthos community but contributes to theremoval of surplus anthropogenic CO2 from the atmosphere through sedimentation andburial of organic and inorganic carbon compounds.It is thus important to increase our comparatively sparse knowledge of all aspectsof zooplankton ecology by a joint eort on the basis of intercomparable methodsfor understanding and predicting the impact of environmental changes on shstocks. We also need to know more about the role of zooplankton in modeling thecycling of biogeochemical key elements such as carbon, nitrogen and phosphorus inthe sea.During the last decade, zooplankton research has gained a fresh impetus as mirroredby the very well attended International Symposium on Zooplankton Production, whichtook place in Plymouth in August 1994 under the auspices of the International Councilfor the Exploration of the Sea (ICES) (Harris 1995). In the keynote lecture, the `pivotalrole of zooplankton' in controlling phytoplankton production and shaping pelagicecosystems was stressed by Banse (1995). The great signicance of zooplankton researchis also recognized in two current large international research programs. Within the JointGlobal Ocean Flux Study (JGOFS) zooplankton plays an important role in regulatingparticle ux to the deep sea. The impact of climatic change on zooplankton populationdynamics inuencing the recruitment success of pelagic sh stocks forms the main focusof Global Ocean Ecosystem Dynamics (GLOBEC).1.2 GENERAL DEFINITIONSThe term `plankton' was coined by the German founder of quantitative plankton andshery research Victor Hensen (1887). It is derived from the Greek word `planao'meaning to wander and it has the same etymological root as `planet'. It embraces allthose organisms drifting in the water whose abilities of locomotion are insucient toICES Zooplankton Methodology Manual Copyright #2000 Academic PressISBN 0-12-327645-4 All rights of reproduction in any form reservedwithstand currents, as opposed to nekton, the community of actively swimmingorganisms such as large crustaceans, cephalopods, shes and aquatic birds andmammals. Although the adjective `planktonic' has been established for a long time andis widely used, a plea is made in favor of the more correct term `planktic' in which thesyllable `on' is deleted. The same problem is correctly solved in the corresponding term`benthic' which is already in wider use than `benthonic'.Although exposed to the forces of turbulence and currents, almost all zooplanktonspecies have developed some means to move, at least to change their vertical positionwithin the water column. Protozoans use either agella and cilia or change their specicweight by ion exchange or incorporation of oil droplets, for instance. Movement by ciliais also common in many invertebrate larvae, for example in polychaete trochophores,mollusks and echinoderm larvae. Medusae and salps move by peristaltic contractions,and lobate ctenophores and pteropods move by apping their lobes and wingsrespectively. Chaetognaths as ambush predators, which catch their prey in one swiftmovement, contract their longitudinal muscles and use their ns. Pelagic polychaetesand crustaceans have developed a large variety of special swimming appendages likeparapodia and swimming legs. Appendicularia use their tails as oar blades. Smallcephalopods employ the same mode of propulsion as the adults and sh larvae alreadypossess rudimentary ns.Zooplankton may be distinguished from phytoplankton either on the basis ofmorphology or mode of nutrition, autotrophic or heterotrophic. From the latterviewpoint zooplankton may be dened as the community of all phagotrophic organisms.According to their food preferences they can be classied as herbivorous, detrivorous,omnivorous or carnivorous. Heterotrophic plankton also include the osmotrophicbacteria, termed bacterioplankton. Mixotrophy, the combination of auto- and hetero-trophy, is quite commonly found in agellates and other protozoans like foraminiferans,radiolarians and ciliates, and it occurs in some metazoan phyla, too, for instance incnidarians and mollusks. A further distinction is made between obligatory and optionalmixotrophy.Species spending their whole life in the pelagic realm are termed holoplanktic asopposed to meroplankton, which drift in the sea only for part of their life cycle. Amongthe protozoans, the majority of agellates and ciliates as well as all pelagic foraminifer-ans and radiolarians belong to the rst group. Also classed in the same group are fromamong the metazoans the siphonophores, ctenophores, pelagic polychaetes, heteropods,pteropods, ostracods, copepods with few exceptions, hyperiids, euphausiids, chaeto-gnaths, appendicularians and salps.Concerning the meroplankton, we distinguish between species which switch over fromplankton to nekton during their juvenile stage, for example cephalopods and sh, andthose which change from a planktic to benthic life and vice versa. Here we nd a largevariety of life strategies. A special case is the life cycle of most hydrozoans andscyphozoa, which exhibit two alternating generations. A summer generation of pelagicmedusae with sexual reproduction is followed by a winter generation of benthic polypswith vegetative propagation.Two contrasting modes of behavior are found among the other meroplankton groups,depending on their main habitat. We have plankton organisms with benthic restingstages and benthos organisms with planktic larvae. Cysts are produced by protozoans,agellates and ciliates, and resting eggs by rotifers, cladocerans and some copepodfamilies (Madhupratap et al. 1996) for surviving unfavorable environmental conditions.Propagation through planktic larvae is found in many benthos groups, for example2 INTRODUCTIONpolychaetes, mollusks, echinoderms, bryozoans, and barnacles and decapods among thecrustaceans. Depending on the time period spent as drifting plankton and theavailability of food, the larvae are either lecithotroph, living o their yolk reserves, orplanktotroph, feeding on phyto- and zooplankton.1.3 SIZE CLASSIFICATIONMarine zooplankton comprises a large variety of dierent organisms with some tenthousands of species if meroplankton is included. Their sizes range from tiny agellates,a few mm large, up to giant jellysh of 2 m diameter, and thus span six orders ofmagnitude. To cope with this enormous size range volume and weight span eighteenorders of magnitude a rst attempt at size classication was already undertaken asearly as 100 years ago in the rst days of quantitative plankton research (Schu tt 1892).He distinguished between micro-, meso- and macrozooplankton. This rst classicationhas since been extended and modied several times. The latest revision (Sieburth et al.1978) is now widely accepted (Figure 1.1).Fig. 1.1 Size spectrum of different taxonomic-trophic compartments of planktonincluding the size range of nekton modified after Sieburth et al. (1978) used withpermission.SIZE CLASSIFICATION 3Zooplankton ranges over ve size classes from nanoplankton to megaplankton. Sincethe nest mesh size of plankton gauze was, for a long time, 20 mm, this value dened thelower boundary of the so-called `net plankton' which could be sampled by plankton nets,neglecting the smaller nano- and picoplankton. For this reason, the size class division (inFigure 1.1) is based on a factor of 2 instead of 1. Each size class covers one order ofmagnitude except mesozooplankton, which covers two orders. This exception is justiedby the fact that the doubled size range corresponds to the size spectrum of traditionalzooplankton samples taken by a mesh size of 200330 mm. Such samples usually containthe bulk of crustacean plankton and, if present, of meroplanktic larvae as well.Moreover, the limits of this size class (0.220 mm) almost exactly match the size rangeof copepodites and adult copepods that generally constitute the dominant zooplanktongroup.The main constituents of nanozooplankton (220 mm) are heterotrophic nanoagel-lates feeding on bacteria. Most other protozoans, especially the ciliates, belong to thenext size class, the microzooplankton (20200 mm). This size class also covers the eggsand early development stages of crustacean plankton and meroplanktic larvae. Smallhydromedusae, ctenophores, chaetognaths, appendicularians, doliolids, sh eggs andlarvae together with the older stages of crustacean plankton and meroplanktic larvaecomprise the mesozooplankton (0.220 mm) already mentioned.In the next two size categories, species numbers diminish. Macrozooplankton (220 cm) are the larger specimens of hydromedusae, siphonophores, scyphomedusae,ctenophores, mysids, amphipods, euphausiids, salps and eel larvae, for instance. Only afew organisms reach the size of megazooplankton (20200 cm). These are mainly largeFig. 1.2 The relationship between organism (particle) size expressed as equivalentspherical diameter and doubling time fromdata for phytoplankton (P), herbivores(Z), invertebrate carnivores or omnivores (I) and fish (F) fromSheldon et al. (1972)modified by Steele (1977) used with permission.4 INTRODUCTIONjellysh, siphonophores and scyphozoa, and pelagic tunicates, pyrosomes and chain-forming salps.Body size is a decisive factor in governing growth rate and doubling time of planktonorganisms. Since within the pelagic food web most predators swallow their preyorganisms undivided, body size also determines food-chain relationships. An examplefor its signicance is the famous diagram by Sheldon et al. (1972) and modied by Steele(1977) as shown in Figure 1.2.The methods described and discussed in this manual deal with net plankton, mainlywith micro-, meso- and macrozooplankton which embrace most of the dominant speciesin meso- and eutrophic ecosystems.1.4 MAIN SYSTEMATIC GROUPSAnother way of classifying planktic organisms is to consider their systematic positionand biochemical composition. The rst step is to distinguish between proto- andmetazooplankton. Among the protozoans the ciliates, especially naked ciliates, formthe ecologically most important group. Their division rate is so rapid as to enable themto almost keep pace with phytoplankton. Thus they react immediately to algal growthand take advantage of the food supply oered. In neritic ecosystems they are often therst grazers of the phytoplankton spring bloom (Smetacek 1981).Characteristic of metazooplankton is a comparatively long life-span, ranging fromseveral days in rotifers and few weeks in small crustaceans to several years in largeeuphausiids in polar regions. A long life-span generally goes hand in hand with along development period. This is most pronounced in crustaceans where in somegroups organisms have to pass through many larval stages before reaching sexualmaturity.Since crustaceans are represented in zooplankton mainly by eight orders, cladocerans,ostracods, copepods, cirripeds, mysids, amphipods, euphausiids and decapods, theseorganisms generally dominate the samples. They are collectively termed crustaceanplankton as opposed to the so-called gelatinous plankton. In the latter group theorganisms are characterized by a gelatinous body, the most prominent representativesbeing the common jellysh (Scyphomedusae). Gelatinous zooplankton comprisesvarious systematic groups, indicating that this particular mode of adaptation to plankticlife in the sea was arrived at through independent evolutionary processes. We refer tocnidarians with hydromedusae, siphonophores and scyphomedusae, the ctenophoresand the pelagic tunicates with pyrsomes, doliolids, salps and appendicularians. Thelatter are included not because of their body constitution but because they havegelatinous houses which are regularly abandoned and rebuilt. Occasionally, a singlespecies in other groups has acquired a gelatinous body too, for example in heteropodsand ostracods. The high water and also salt content of these organisms causes asubstantial shift in the ratio between organic matter content and wet weight, dry weightand inorganic matter content as compared with crustacean plankton, for instance. Itfurther enables gelatinous species to grow very fast manifested by the huge swarmsfrequently encountered.Other ecologically important groups, not belonging to crustacean or gelatinousplankton, are rotifers in brackish waters, pteropods, chaetognaths, and especially shlarvae.MAIN SYSTEMATIC GROUPS 51.5 SPECIES DIVERSITYTable 1.1 gives an overview of the main marine zooplankton groups with theirapproximate species numbers. The gures in brackets are very rough estimates sincerelevant data are lacking. This is especially true of the meroplanktic larvae, whereestimates rely on the number of the parental benthos and nekton species. The guresquoted may therefore give only an idea of the vast species diversity in these groups.Summing up the gures listed in Table 1.1, one arrives at a total of around 36 000 species.Holoplankton with about 6000 protozoan (16%) and about 4000 metazoan species(11%) makes up roughly a quarter (27%). The bulk (73%) consists of the lesser knownmeroplankton with uncertain estimates, and the total should therefore be taken as only atentative measure of the order of magnitude.In most aspects of zooplankton research, accurate species identication is a necessarybut often not easily achievable prerequisite. The help of experts in systematics might beneeded. Even if only the biomass distribution is investigated during a survey by applyingbulk methods like volume or weight measurements, at least a rough inspection of themain species composition would provide valuable information.A rst impression of the vast diversity of zooplankton organisms may be obtainedfrom the excellent drawings by the Scottish planktologist James Fraser (1962),reproduced in Figures 1.41.16 at the end of this chapter. The following contains ashort but in no way exhaustive list of introductory guides, plankton books, identicationsheets and recent monographs on various zooplankton taxa.There exist several introductory guides which are well written and contain a largenumber of informative drawings. Newell and Newell (1973) present boreal plankton,Wickstead (1965) tropical plankton and Tregoubo and Rose (1957) subtropicalplankton in the Mediterranean Sea. Todd and Laverack (1991) provide a specialintroduction to neritic boreal zooplankton, this diers from other guide books inpresenting photographs of preserved specimens as encountered by the normal investi-gator. Two very readable and well illustrated books which give a general account of thelife of North Atlantic plankton are Fraser's (1962) Nature adrift and Hardy's (1970)World of plankton, whereas Raymont's (1983) Zooplankton is recognized as a compre-hensive textbook.The identication sheets, edited by ICES since 1947, are a collection of leaets dealingwith all zooplankton taxa from Foraminifera to sh larvae occurring in the northeastAtlantic and its adjacent seas. Most of them contain an identication key and table ofgeographical distribution. A table of contents of the sheets is found in Todd andLaverack (1991).The monographs listed below also include accounts of the biology of variouszooplankton groups. Dinoagellates (Taylor 1987) play an important role in thesystematically diverse group of heterotrophic agellates. Ciliates are described by Corliss(1979), Foraminifera by Hemleben et al. (1989) and Radiolaria by Anderson (1983). TheHydro- and Scyphomedusae are presented by Russell (1953, 1970) in two volumes.Siphonophores are dealt with by Alvarin o (1971) and Mackie et al. (1987) andctenophores by Reeve and Walter (1978). An account of boreal meroplanktic larvae,especially of polychaetes and mollusks, is given by Thorson (1946). Heteropoda aredescribed by Tesch (1949) and Pteropoda by Pruvot-Fol (1942) and Tesch (1946, 1948,1950). Juvenile cephalopods are treated by Sweeney et al. (1992).Details on the crustacean plankton are found in the following monographs: Cladocera(Eglo et al. 1997), Ostracoda (Angel 1993), Copepoda (Rose 1933; Marshall and Orr6 INTRODUCTIONTable 1.1 Systematic overview of the main zooplankton taxa with approximatespecies numbers (figures in brackets are very rough estimates), plankton status (holo-or meroplankton) and size class distribution (cf. Figure 1.1). Crosses indicate thedistribution: rare +, common ++, dominant +++.Systematic groupsHolo^MeroPlanktonNano2^20m mmMicro20^200m mmMeso0.2^20mmMacro2^20cmMega20^200cmProtozooplanktonHeterotrophic Flagellates (600) +++ +++ +++ +Ciliata (1000) +++ + +++ +Foraminifera (Globigerina) 30 +++ ++ ++Radiolaria 4500 +++ + +++ +MetazooplanktonCnidariaHydromedusae (500) + +++ ++ ++ +Siphonophora 150 +++ + ++ +Scyphomedusae 250 + +++ + ++ ++Ctenophora 80 +++ + ++ +Rotatoria (100) +++ ++ ++Polychaeta (100) +++ ++ ++ +Polychaeta Larvae (3000) +++ + ++MolluscaHeteropoda 30 +++ ++ ++Pteropoda 100 +++ +++ +Cephalopoda 500 + +++ ++Veliger Larvae (10 000) +++ + +++CrustaceaCladocera 30 + +++ +++Ostracoda 350 +++ +++ +CopepodaCalanoida 1200 +++ + + +++Cyclopoida 100 +++ + +++Harpacticoida 100 +++ + +++Cirripedia Larvae (800) +++ + +++Mysidacea 600 +++ ++ ++ +Amphipoda (Hyperiidea) 300 +++ +++ +Euphausiacea 90 +++ ++ ++Decapoda 200 +++ + +++Decapoda Larvae (6000) +++ +++ +Echinodermata Larvae (2000) +++ +++Chaetognatha 50 +++ ++ ++TunicataCopelata 60 +++ +++ + +Thaliacea 45 +++ ++ ++ +Fish Larvae (3000) +++ +++ +SPECIES DIVERSITY 71955; Mauchline 1998), Cirripedia (Southward 1987; Anderson 1994), Mysidacea(Mauchline 1980), Hyperiidea (Bowman and Gruner 1973; Vinogradov et al. 1996),Euphausiacea (Mauchline and Fisher 1969; Mauchline 1980), Decapoda (Omori 1974;Dall et al. 1990) and decapod larvae (Gurney 1939). Chaetognaths are described byAlvarin o (1965) and Pierrots-Bults and Chidgey (1988). Pelagic tunicates are treated byFraser (1981) and Bone (1997) and sh larvae by Fahey (1983) and Moser et al. (1984).1.6 ECOLOGICAL POSITIONThe ecological role of an organism is largely determined by its position andsignicance in the food web. Decisive characteristics are body size, food spectrum andfeeding type. Filter-feeders like copepods, euphausiids and pelagic tunicates, feeding ondierent size spectra of phytoplankton, organic detritus as well as on nano- andmicrozooplankton, are primarily herbivores and omnivores. As secondary producersthey thus occupy the second and to some extent third level in the food web. Various ltertechniques are employed. Copepods and euphausiids use their highly structuredmouthparts and feeding appendages, appendicularians a ne-meshed funnel net insidetheir house and thaliaceans a ciliary mucous net inside their barrel-shaped body.Ciliates, rotifers and many meroplankton larvae feed by means of ciliary currents.Thecosome pteropods employ large mucous nets for trapping their prey.Raptional feeders are typically predators. Cnidarians and ctenophores catch their preywith stinging or sticky tentacles. Pelagic polychaetes, heteropods, gymnosome pteropodsand cephalopods among the mollusks, hyperiids (amphipods) and sh larvae may beregarded as active hunters, whereas chaetognaths are described as ambush predators.Cladocerans, ostracods and mysids occupy an intermediate position between thetypical lter-feeding and the raptional zooplankton. It should, however, be stressed thatthe above classication has no strict demarcations, since there exist many exceptions invarious groups. Ciliates, for instance, have carnivorous members feeding on their ownrelatives. Some scyphomedusae (Hansson 1997) and ctenophores (Greve 1981) prefer toprey on related species. Similarly in pteropods, gymnosomes feed on thecosomes. Thereare quite a number of carnivorous species among copepods and euphausiids too, andeven a very typical lter-feeder like Calanus nmarchicus is able to switch to raptorialfeeding, at least under laboratory conditions.Because of their worldwide distribution, abundance and dominance, the followingthree groups may be regarded as the most signicant secondary producers, the nakedciliates among the protozoa, and the copepods and euphausiids among the metazoa,both the latter specially in boreal and polar regions. Appendicularians and salps are alsoof importance in some areas, but their occurrence is of a more seasonal character andthey are not as ubiquitous as the former groups. Ctenophores can have a high ecologicalimpact as predators, as has been demonstrated in the Black Sea by the recentlyintroduced species Mnemiopsis leidyi (Harbison 1994). Scyphomedusae like Aureliaaurita can function as top predators in inshore seas and structure the food web by top-down control (Behrends and Schneider 1995).The functioning of food webs depends on the balance between bottom-up and top-down control. Bottom-up is the resource-driven control. In the pelagic realm, it isprimarily exercised by the supply of nutrients determining the amount of primaryproduction. Recently, the pivotal role of zooplankton grazing in controlling phyto-plankton growth has been stressed (Banse 1995) in explaining the apparent paradox of8 INTRODUCTIONthe so-called `high' nutrient `low' chlorophyl regions. A high grazing pressure byherbivores prevents phytoplankton blooms.The top-down control is particularly marked in the microbial food web, where ciliatesare the top predators. They themselves are controlled by lter-feeding metazooplankton,thus connecting the microbial with the classical food web (Figure 1.3). Both food webtypes coexist in all areas of the ocean, but their relative signicance changes with regionand season. The classical food chain dominates in eutrophic cold-water and upwellingecosystems. The microbial food web, however, is most signicant in oligotrophic warm-Fig. 1.3 Simplified food web structure with microbial loop, microbial food web andclassical food chain. Microbial food web includes microbial loop and autotrophicpicoplankton and nanoplankton 55 mm. (DOC =dissolved organic carbon andHNF =heterotrophic nanoflagellates.) Modified after Lenz (1992) used withpermission.ECOLOGICAL POSITION 9water systems and during summer stratication in nutrient-depleted surface waters inhigher latitudes (Lenz 1992).1.7 DISTRIBUTION PATTERNZooplankton distribution is governed by water depth, trophic status of the area andtemperature regime, to mention the most important factors. Water depth separatesneritic from oceanic plankton. Neritic plankton inhabits inshore waters up to about200 m at the shelf edge. Characteristic of neritic plankton is a high proportion ofmeroplankton larvae and species with benthic resting eggs. The proximity to the seabottom favors an exchange between plankton and benthos communities.Oceanic zooplankton on the other hand is characterized by a general absence ofmeroplankton and the presence of distinct vertical migrators. Among them are, forinstance, larger copepod species and euphausiids. The daily migration, rising at dusk anddescending at dawn, often extends over several hundred metres. Seasonal verticalmigration as exhibited by many members of the copepod genus Calanus in higherlatitudes even reaches down to depths of 5001000 m. The epipelagic (0200 m) andmesopelagic zones (2001000 m) are the main domain of zooplankton. Below 1000 mdepth in the bathypelagical, their concentration generally decreases logarithmically withdepth (Vinogradov 1997).Species diversity is generally governed by temperature regime and evolutionary age ofocean areas. The highest diversity is thus found in tropical and subtropical regions andthe lowest in extreme environments such as polar zones and brackish water areas. Due tothe steady water exchange through ocean currents many species enjoy a wide and ofteneven worldwide distribution within their climatic boundaries. This is especially true forthe warm-water sphere comprising all three oceans. Sporadic occurrences of neriticspecies observed since the turn of the century in increasing numbers are now generallyexplained by the high amount of ballast water transported and discharged all over theworld by international ship trac (Carlton and Geller 1993).In studying the distribution and seasonal cycle of marine zooplankton, one is alwaysfaced with the problem that the sea is a highly dynamic environment with a steadymotion and mixing of water masses. Whereas a limnologist, working in a small ormedium-sized lake, can be almost certain of dealing with the same population during aninvestigation period, this is more the exception than the rule for a marine planktologistworking in the sea. Because of prevailing currents and advection of new water masses, itis often virtually impossible to follow the same population of organisms (Huntley andNiiler 1995). Observations at a xed station therefore generally represent a mixture of`sequences' of dierent plankton populations passing by and `seasonal changes' of thesame populations. Every plankton sampling program should be accompanied by adetailed oceanographic documentation, especially salinity measurements and increas-ingly use of hydrodynamic and particle-tracking models, for identifying the impact ofwater mass changes (Chapter 2).1.8 GROWTH AND METABOLISMGrowth and metabolism of zooplankton organisms are governed by the interaction ofa number of forces which may be either internal or external. Internal factors are body10 INTRODUCTIONsize and physiological properties, such as range of temperature tolerance, developmentalstage and physiological state. Feeding activity, for instance, depends on the moltingcycle in crustaceans. External factors are food supply and nutritional properties of food,as well as various environmental factors such as temperature, salinity and oxygensaturation. One must distinguish between potential growth rate under optimal condi-tions and actual growth rate which is often reduced by one or more of the factorsmentioned above. An additional factor aecting population growth is top-down controlthrough predation.Metabolism as well as growth rate is an allometric function of body size. Smallorganisms have a comparatively higher metabolic rate and grow faster than large ones.This allometric relationship is described by the general equationR=aWb(1.1)R stands for respiration or any other metabolic rate including growth. W is body size,usually measured as dry weight, and a and b are constants. Whereas a depends onphysiological properties of the organisms and environmental conditions, b is a uniformconstant attaining the approximate value of 0.75 (Peters 1983). An increase in body size,expressed as volume or weight, by a factor of 1000, which corresponds to a ten-foldincrease in body length, results in a reduction of metabolic rate by a factor of 5.6. Thisvalue gives an idea of the dierence in growth rate between members of two neighboringsize classes, for example microzooplankton and mesozooplankton.Among the external factors governing growth, food supply and temperature are mostimportant. The availability of food varies with season in higher latitudes. Thus themajority of organisms have adapted their life cycle in such a way that they encounteroptimal conditions during their reproduction period.There is also a relationship between food supply and energy conversion. The sparserthe food the better the digestion. During phytoplankton blooms `superuous feeding'has been observed in herbivorous copepods. Their feces contained many undigestedphytoplankton cells. In considering energy conversion it is advisable to distinguishbetween physiological eciency in individual organisms and ecological eciencyexpressing food chain eciency. The rst may be more than twice as high as the latter,where generally only a section of secondary producers, for example herbivorouscopepods, are related to total primary production.Water temperature in the open sea ranges from about 72 8C to approximately 32 8C.Zooplankton organisms inhabit all regions of the sea according to their physiologicaltemperature adaption and tolerance limits. These may be narrow, stenotherm, as inpolar and deep-sea plankton, or eurotherm, as in temperate and neritic waters of higherlatitudes. Within the given tolerance limits of individual species, and within the wholerange of sea temperature for the total plankton community, the intensity of all vitalprocesses depends on the prevailing temperature conditions. This temperature depen-dency is based on the reaction speed of physicochemical processes in living organismsand is described by the van't Ho law or the so-called Q10 rule. For a temperature rise of10 8C, an increase in metabolic rate of two to three times is generally observed (Schmidt-Nielsen 1979). Special adaptations to extreme temperatures in polar seas, for instance,are possible to some degree, but the general validity of this rule for all poikilothermorganisms is not suspended.Knowing body size, developmental stage and physiological state of a planktonorganism and the temperature conditions, it is thus possible to calculate the potentialgrowth rate. In marine copepods, where dominant species often vary comparatively littleGROWTH AND METABOLISM 11in body size, temperature has been demonstrated as the main factor governing theirgrowth rate (Huntley and Lopez 1992).Physical stress factors such as reduction in salinity and oxygen content limit speciesdistribution and diminish growth and body size in those species which are able totolerate these adverse environmental conditions. Thus brackish water organisms areusually smaller than their marine relatives because of the extra energy spent inphysiological adaption.Assimilated energy is converted both into somatic growth and egg production. Femalecopepods on reaching the adult stage after the last molting spend all their surplus energyon egg production. Thus egg production replaces somatic growth. Special methods havebeen developed to measure egg production in order to include it in estimates ofzooplankton production.1.9 REPRODUCTION AND DEVELOPMENTVegetative propagation through binary ssion predominates in protozooplankton,whereas sexual reproduction is the common mode of propagation in metazooplankton.There are, however, quite a number of exceptions from this rule. The pelagic foramini-fera, the Globigerina, multiply, for instance, by multiple ssion, producing eithervegetative cells or agellated gametes. Vegetative propagation through budding occursin hydromedusae and is a regular part of the life cycle of thaliaceans.Parthenogenesis, the asexual propagation through unfertilized eggs, is a specialachievement in rotifers and cladocerans. After a period of propagation throughparthenogenesis a sexual generation appears in which the females produce fertilizedeggs. These are protected by a thick shell and hibernate on the sea bottom untilparthenogenic females hatch in spring.Vegetative propagation and parthenogenesis have the great ecological advantage thata large population can be built up in a short period. These organisms are thus able tooptimally utilize favorable feeding conditions.Equally advantageous is a direct development from egg or rst larval stage to adult, aswe have with the ephyra in scyphomedusae. Such a development, which is found inctenophores, ostracods and chaetognaths, for instance, is usually much faster thanpassing through a number of dierent larval stages, as is typical for copepods andeuphausiids. Copepods have to pass six naupliar and ve copepodite stages beforemolting into adults.1.10 STANDING STOCK AND PRODUCTIONThe relationship between standing stock and production of a population depends onfood supply and climatic conditions and varies largely with season in most areas. Thestronger the seasonal impact, generally the greater the variation. A very decisive factor isthe temperature governing the growth rate. In cold-water ecosystems dominant speciesneed to maintain a relatively high biomass to assert their predominance, since produc-tion rate is slow. In warm-water ecosystems it is possible to build up a large populationfrom a low standing stock because of the high growth rate. The ratio between productionand biomass of a species is an important index of its population dynamics and indicatesthe turnover rate of organic matter. Under optimal food conditions, the highest turnover12 INTRODUCTIONrate is thus observed in small organisms in the tropics and the lowest in large organismsin polar regions.Many zooplankton species, especially those in cold-water and upwelling ecosystems,have developed various life strategies to adjust their growth and reproduction period tooptimal environmental conditions. One mode of adaption to cope with unfavorableseasonal conditions is to produce resting eggs, as already mentioned. It is common incladocerans and also occurs in a number of neritic copepod species (Madhupratap et al.1996; Williams-Howze 1997). Another strategy is the evolution of a diapause stage asobserved in members of the genus Calanus and its relatives, where copepodite stages IVand V, after having accumulated a large lipid reserve, migrate down to great depths anddrift there motionless until the beginning of the next growth season.1.11 CONCLUSIONWhen measuring zooplankton biomass and estimating its production, one usuallytends to deal with the whole community. By employing dierent mesh sizes in nets andsieves it is possible to separate the main components from each other, for instancemicrozooplankton from mesozooplankton or small herbivores from larger carnivores bymeans of size fractionation. This approach may occasionally prove quite successful,depending on the size spectra and diversity of the species. Bulk parameters obtained inthis way may provide useful data for modelers. It is, however, always necessary to realizethat such data are no more than a methodological compromise, for reality is far morecomplex. The trophic role and ecological signicance of zooplankton communitiesdepends on the diversity, behavior and interaction of their species. These communitiesare often dominated by so-called key taxa, which play the main role in channeling energyup the food web and exercising top-down control through grazing or predation. Futureresearch should put more emphasis on special environmental adaptations of thesepredominant species and their ecological signicance in forming the food web (Verityand Smetacek 1996).CONCLUSION 13Fig. 1.4 Protozoa. See page 27 for key.14 INTRODUCTIONFig. 1.5 Small jellyfish. See page 27 for key.INTRODUCTION 15Fig. 1.6 Large jellyfish. See page 27 for key.16 INTRODUCTIONFig. 1.7 Other Coelenterates etc. See page 27 for key. Scale lines all represent 1 cm.INTRODUCTION 17Fig. 1.8 Various kinds of zooplankton. See page 27 for key.18 INTRODUCTIONFig. 1.9 Various planktonic Crustacea etc. See page 27 for key.INTRODUCTION 19Fig. 1.10 Calanoid copepods. See page 28 for key.20 INTRODUCTIONFig. 1.11 Crustacean larvae etc. See page 28 for key.INTRODUCTION 21Fig. 1.12 Crustaceans. See page 28 for key.22 INTRODUCTIONFig. 1.13 Planktonic Tunicata. See page 28 for key.INTRODUCTION 23Fig. 1.14 Planktonic larvae of various invertebrates. See page 29 for key.24 INTRODUCTIONFig. 1.15 Planktonic stages of polychaete worms. See page 29 for key.INTRODUCTION 25Fig. 1.16 Echinoderm larvae etc. See page 29 for key.26 INTRODUCTIONCaptions for Figures 1.4^1.9.Fig. 1.4 ProtozoaCiliata: (1) Vorticella marina, (2a) Zoothamnion marinum, (2b) at a reduced scaleshowing colonies on the copepod Eurytemora hirundoides, (3) Cothurnia gracilis,(4) Cothurnia havniensis, (5) Epiclintes retractilis, (6) Aegyria monostyla, (7) Euplotesharpa, (8) Aegyria oliva, (9) Amphisia pernix, (10) Stichochaeta pediculiformis,(11) Oxytricha pellionella. Suctoria: (12) Acineta tuberosa. T|ntinnoidea:(13) Parafavella elegans, (14) Parafavella edentata, (15) Ptychocylis minor,(16) Salpingella ricta, (17) T|ntinnus tubulosus, (18) Dictyocysta magna. Radiolaria:(19) Challengeron neptuni, (21) Acanthometron pellucidum, (24) Acanthochiasmafusiforme, (25) Hexalonche philosophica. Foraminifera: (20) Nonion pompilioides,(22) Globigerina bulloides. Silicoflagellata: (23) Dictyocha fibula, (26) Distephanusspeculum, (27) Thalassicola nucleata. All to the same scale except (2b) and (27) (Fraser1962) used with permission.Fig. 1.5 Small jellyfish(1) Hybocodon profiler, (2) Sarsia tubulosa, (3) Dipurena ophiogaster, (4) Podocoryneborealis, (5) Leuckartiara octona, (6) Bougainvillia principis, (7) Amphinema rugosum,(8) Eutima gracilis, (9) Eutonina indicans, (10) Aglantha digitale. (2), (3), (4), (6) and(7) to the same scale as (1); (8)^(10) to the same scale as (5) (Fraser 1962) used withpermission.Fig. 1.6 Large jellyfish(1) The pearl jelly, Pelagia noctiluca, (2) Chrysaora hyoscella, (3) the big stinger orlion's mane, Cyanea, (4) the cauliflower jelly Rhizostoma octopus, (5) the moon jellyAurelia aurita. (1) Rarely exceeds 3 inches, (5) reaches about 1 foot, but the othersmay occasionally be up to 3 feet across (Fraser 1962) used with permission.Fig. 1.7 Other Coelenterates etc.Siphonophores or pseudo-siphonophores: (1) Chelophyes appendiculata, (2)Physophora hydrostatica, (3) Agalma elegans, (4) Physalia physalis, the Portugueseman o' war, (5) Velella velella, the by-the-wind sailor. Ctenophores (comb-jellies):(6) Pleurobrachia pileus, the sea gooseberry, (7) Beroe cucumis. (8) A larva of the sea-anemone Cerianthus, called Arachnactis larva. (9) A pelagic polychaete worm,Tomopteris helgolandica. The scale lines all represent 1 cm(Fraser 1962) used withpermission.Fig. 1.8 Various kinds of zooplanktonHarpacticoid and cylopoid copepods: (1) Microsetella norvegica, (2) T|griopus fulvus,(3) Idya furcata, (4) Oithona similis. Chaetognatha: (5) Sagitta elegans. Pteropoda(shells): (6) Clio pyramidata, (7) Spiratella (=Limacina) retroversa, (8) Spiratellahelicina, (9) Clione limacina. Small Cephalopoda: (10) Sepiola, (11) Brachiotheuthis.The arrow in (4) indicates the joint between the cephalosome and abdomen (Fraser1962) used with permission.Fig. 1.9 Various planktonic Crustacea etc.Cladocera: (1) Podon leuckartii, (2) Evadne nordmanni. Ostracoda: (3) Conchoeciaelegans. Insecta: (4) Halobates micans. Amphipoda: (5) Themisto abyssorum,(6) Hyperia galba male (the female is much broader). Isopoda: (7) Eurydice pulchra,(8) Idothea balthica. Copepoda: (9) Caligus rapax, the sea louse, a semi-parasiticcopepod. Cumacea: (10) Dyastylis rathkei (Fraser 1962) used with permission.INTRODUCTION 27Captions for Figures 1.10^1.13.Fig. 1.10 Calanoid copepods(1) Pseudocalanus elongatus, (2) Centropages typicus, (3) Acartia longiremis,(4) Temora longicornis, (5) Eurytemora hirundoides, (6) Calanus finmarchicus,(7) Metridia lucens, (8) Candacia armata, (9) Pareuchaeta norvegica, (10) Anomalocerapatersoni male, (11) female. The arrow in (1) indicates the joint between thecephalosome and abdomen (Fraser 1962) used with permission.Fig. 1.11 Crustacean larvae etc.Copepoda: (1a) and (1b) 1st and 3rd stages of the nauplius of T|griopus, (2) 4thnauplius of Calanus, (3) 5th nauplius of Centropages, (4) 5th nauplius of Oithona.Cirripedia: (5) 2nd nauplius of acorn barnacle, Balanus, (6) cypris stage of same,(7) adult goose barnacle, Lepas. Decapoda: (8) 3rd zoea of crab, Portunus puber,(9) megalopa of same, (12) phyllosome of spiny lobster, Palinurus. Euphausiacea:(10) 2nd nauplius of Thysanoessa inermis, (11) 2nd calyptopis of Thysanoessalongicaudata (Fraser 1962) used with permission.Fig. 1.12 CrustaceansMysidacea: (1) Gnathophausia zoea, (2) Gasterosaccus sanctus. Amphipoda:(3) Mimonectes loverni, an exotic species. Euphausiacea: (4) Thysanoessa inermis,(5) Meganyctiphanes norvegica. Larvae of various Decapoda: (6) Sergestes, an oceanicprawn, (7) and (8) Eupagurus, hermit-crab, (9) Pontophilus, (10) Nephrops, Norwaylobster, (11) Porcellana, pea-crab, (12) Crangon, shrimp, (13) Galathea, (14) Munida,squat lobster (Fraser 1962), used with permission.Fig. 1.13 Planktonic TunicataAppendiculata: (1) Oikopleura dioica, (2) Fritillaria borealis. Thaliacea: (3) Thaliademocratica, solitary stage showing the budding stolon (a) which gives rise to a chainof aggregate stages, (4) Thalia democratica, aggregate stage with a single embryo (b)which will eventually become a free solitary stage, (5) Salpa fusiformis, aggregatestage, (6) Salpa fusiformis, solitary stage, with stolon, (7) Dolioletta gegenbauri,gonozoid, complete with sexual organs. The eggs from this stage hatch into`tadpoles'. (8) A later stage of the `tadpole' showing the remains of the outer capsuleand the oozoid developing inside, (9) the late oozoid or `old nurse' now devoid ofalmost all its internal organs, but with broad muscle bands and balancing organ(statocyst), a nerve center and the remains of the dorsal process, (10) a view fromabove of the oozoid at its functional stage with a prominent dorsal process, (a) thebuds developing on the stolon, (b) the buds migrating to the dorsal process, (c)double rows of lateral zooids, the trophozoids which serve only to catch food for thewhole, (d) median rows of phorozoids, and (e) the youngest migrating buds whichwill become new gonozoids, (11) a later stage of a phorozoid, now broken free fromthe dorsal process of the oozoid and acting as a bearer for two developing gonozoids.These will eventually become the free living sexual formfigured in (7) (Fraser 1962)used with permission.28 INTRODUCTIONCaptions for Figures 1.14^1.16Fig. 1.14 Planktonic larvae of various invertebrates(1) Pilidium larvae of nemertine worm, (2) Actinotrocha larva of Phoronis, (3)Cyphonautes larva of a sea moss, Membranipora. Gasteropoda (univalve mollusks):(4) Nassarius reticulata, (a) larva just after hatching, (b) old larva with shell forming,(5) Nassarius incrassata, old larva, (6) Actis minor, old larva with shell forming, (7)Littorina littorea (periwinkle), (a) young larva, (b) later larva. Lamellibranchiata(bivalve mollusks): (8) Tellina sp., (9) Macoma baltica, (10) Cardium edule (cockle),(11) Mytilus edulis (mussel), (12) Pecten opercularis (queen, or small scallop). (1)^(7)from Thorson, (8)^(12) from Jrgensen (Fraser 1962) used with permission.Fig. 1.15 Planktonic stages of polychaete worms(1) Autolytus prolifer, with eggs, (2) Harmothoe imbricata, (a) metatrochophore, (b)nectochaete stage, (3) Phyllodoce groenlandica, old trochophore, (4) Phyllodocemaculata, old larva, (5) Nereis pelagica, nectochaete stage, (6) Nephthys ciliata, (a)young trochophore, (b) and (c) metatrochophores, (7) Polydora coeca, old larva, (8)Pygospio elegans, old larva, (9) Myriochele danielsseni, young larva, (10) Nephthyscoeca, nectochaete stage, (11) Megalona papillicornis, old larva, (12) Pectinariaauricoma, (a) young larva, (b) old larva in a gelatinous tube, (13) Lanice conchilega,old larva in a gelatinous tube. All from Thorson (Fraser 1962) used with permission.Fig. 1.16 Echinoderm larvae etc.(1) Bipinnaria larva of a starfish, Asterias glacialis, (2) Brachiolaria larva of Asteriasrubens, (3) Auricularia larva of a sea cucumber, Synapta digitata, (4) Doliolaria larva,or pupa, of Synapta, (5) Pluteus larva of a brittle star, Ophiura texturata, (6) Pluteuslarva of a brittle star, Ophiothrix fragilis, (7) Pluteus larva of a sea urchin,Echinocardium cordatum, (8) Tornaria larva of the acorn-worm, Balanoglossus(Hemichordata). (1)^(4) are to same scale (Fraser 1962) used with permission.INTRODUCTION 291.12 REFERENCESAlvarin o, A., 1965. Chaetognaths. Oceanography and Marine Biology: an Annual Review,3: 115194.Alvarin o, A., 1971. Siphonophores of the Pacic with a review of the world distribution.Bulletin of the Scripps Institution of Oceanography, 16: 1432.Anderson, D.T., 1994. Barnacles: structure function, development and evolution. Chapman &Hall, London, 357 pp.Anderson, O.R., 1983. Radiolaria. Springer, New York, 355 pp.Angel, M.V., 1993. Marine planktonic ostracods. Synopses of the British Fauna (New Series)No. 48. Limnean Society, London, 239 pp.Banse, K., 1995. Zooplankton: Pivotal role in the control of ocean production. ICES Journalof Marine Science, 52: 265277.Behrends, G. and Schneider, G., 1995. Impact of Aurelia aurita medusae (Cnidaria,Scyphozoa) on the standing stock and community composition of mesozooplankton inthe Kiel Bight (western Baltic Sea). Marine Ecology Progress Series, 127: 3945.Bone, Q. (ed.), 1997. The biology of pelagic tunicates. Oxford University Press, Oxford,340 pp.Bowman, T.E. and Gruner, H.E., 1973. The families and genera of Hyperiidae (Crustacea:Amphipoda). Smithsonian Institution Press, Washington, USA, 64 pp.Carlton, J.T. and Geller, J.B., 1993. Ecological roulette: the global transport of non-indigenous marine organisms. Science, 261: 7882.Corliss, J.O., 1979. The ciliated protozoa, 2nd edition. Pergamon Press, Oxford, 455 pp.Cushing, D.H., 1990. Plankton production and year-class strength in sh-populations:an update of the match/mismatch hypothesis. Advances in Marine Biology, 26: 249293.Dall, W., Hill, B.J., Rothlisberg, P.C. and Sharples, D.J., 1990. The biology of the Penaeidae.Advances in Marine Biology, 28: 1461.Eglo, D.A., Fofono, P.W. and Onbe , T., 1997. Reproductive biology of marine cladocera.Advances in Marine Biology, 31: 79167.Fahay, M.P., 1983. Guide to the early stages of marine shes occurring in the western NorthAtlantic Ocean, Cape Hatteras to the southern Scotian Shelf. Journal of NorthwestAtlantic Fishery Science, Dartmouth, Canada, 4: 423 pp.Fraser, J., 1962. Nature adrift. The story of marine plankton. G.T. Foulis, London, 178 pp.Fraser, J.H., 1981. British pelagic tunicates. Cambridge University Press, London, 57 pp.Greve, W., 1981. Invertebrate predator control in a coastal marine ecosystem: the signicanceof Beroe gracilis (Ctenophora). Kieler Meeresforschungen, Sonderheft, 5: 211217.Gurney, R., 1939. Bibliography of the larvae of decapod Crustacea. London (reprinted 1960,Engelmann, Weinheim, Germany), 306 pp.Hansson, L.J., 1997. Capture and digestion of the scyphozoan jellysh Aurelia aurita byCyanea capillata and prey response to predator contact. Journal of Plankton Research, 19:195208.Harbison, G.R., 1994. The ctenophore Mnemiopsis leidyi in the Black Sea: a holoplanktonicorganism transported in the ballast water of ships. Proceedings of NOAA Conference: 2536.Hardy, A., 1970. The open sea: Its natural history. Part I: The world of plankton, 2nd edition.Collins, London, 335 pp.Harris, R. (ed.), 1995. ICES Symposium `Zooplankton Production' 1994. ICES Journal ofMarine Science, 52: 261773.30 INTRODUCTIONHemleben, C.H., Spindler, M. and Anderson, O.R., 1989. Modern planktonic foraminifera.Springer, New York, 363 pp.Hensen, V., 1887. Uber die Bestimmung des Planktons oder des im Meere treibenden Materialsan Panzen und Tieren. V. Bericht der Commission zur wissenschaftlichen Untersuchungder deutschen Meere in Kiel. Paul Parey, Berlin, 108 pp.Huntley, M.E. and Lopez, D.G., 1992. Temperature dependent production of marinecopepods: a global synthesis. American Naturalist, 140: 201242.Huntley, M.E. and Niiler, P.P., 1995. Physical control of population dynamics in theSouthern Ocean. ICES Journal of Marine Science, 52: 457468.ICES 1947 (continued). Fiches d'Identication du Zooplankton. International Council forthe Exploration of the Sea (ICES), Copenhagen.Lenz, J., 1992. Microbial loop, microbial food web and classical food chain: their signicancein pelagic marine ecosystems. Archiv fu r Hydrobiologie, Beiheft, Ergebnisse der Limnolo-gie, 37: 265278.Mackie, G.O., Pugh, P.R. and Purcell, J.E., 1987. Siphonophore biology. Advances in MarineBiology, 24: 97262.Madhupratap, M., Nehring, S. and Lenz, J., 1996. Resting eggs of zooplankton (Copepodaand Cladocera) from the Kiel Bay and adjacent waters (southwestern Baltic). MarineBiology, 125: 7787.Marshall, S.M. and Orr, A.P., 1955. The biology of a marine copepod, Calanus nmarchicus(Gunnerus). Oliver and Boyd, Edinburgh, 188 pp.Mauchline, J., 1980. The biology of mysids and euphausiids. Advances in Marine Biology, 18:1637.Mauchline, J., 1998. The biology of calanoid copepods. Advances in Marine Biology, 33: 1710.Mauchline, J. and Fisher, L.R., 1969. The biology of euphausiids. Advances in MarineBiology, 7: 1454.Moser, H.G., Richards, W.J., Cohen, D.M., Fahay, M.P., Kendall, Jr., A.W. and Richard-son, S.L., 1984. Ontogeny and systematics of shes. Special Publications No 1, AmericanSociety of Ichthyologists and Herpetologists, Allan Press, Lawrence, USA, 760 pp.Newell, G.E. and Newell, R.C., 1973. Marine plankton. A practical guide. Revised edition,Hutchinson (Educational) Biological Monographs, London, 244 pp.Omori, M., 1974. The biology of pelagic shrimps in the oceans. Advances in Marine Biology,12: 233324.Peters, R.H., 1983. The ecological implications of body size. Cambridge University Press,Cambridge, 329 pp.Pierrots-Bults, A.C. and Chidgey, K.C., 1988. Chaetognatha. Keys and notes for theidentication of the species. Synopses of the British Fauna (New Series) No 39. LimneanSociety, London, 66 pp.Pruvot-Fol, A., 1942. Les gymnosomes. I. Dana-Report No. 20. C.A. Reitzels, Copenhagen,54 pp.Raymont, J.E.G., 1983. Plankton and productivity in the oceans. Zooplankton, 2nd edition,vol. 2. Pergamon Press, Oxford, 824 pp.Reeve, M.R. and Walter, M.A., 1978. Nutritional ecology of ctenophores a review of recentresearch. Advances in Marine Biology, 15: 249287.Rose, M., 1933. Copepodes pelagiques. Faune de France, vol. 26. Paul Lechevalier, Paris,374 pp.Russell, F.S., 1953 and 1970. The medusae of the British Isles, vols. 1 and 2, CambridgeUniversity Press, 528 and 271 pp.REFERENCES 31Schmidt-Nielsen, K., 1979. Animal physiology: adaption and environment, 2nd edition.Cambridge University Press, Cambridge, 560 pp.Schu tt, F., 1892. Analytische Planktonstudien. Lipsius and Tischer, Kiel, 117 pp.Sheldon, R.W., Prakash, A. and Sutclie, Jr., W.H., 1972. The size distribution of particles inthe ocean. Limnology and Oceanography, 17: 327340.Sieburth, J. McN., Smetacek, V. and Lenz, J., 1978. Pelagic ecosystem structure: hetero-trophic compartments of the plankton and their relationship to plankton size fractions.Limnology and Oceanography, 23: 12561263.Smetacek, V., 1981. The annual cycle of protozooplankton in Kiel Bight. Marine Biology, 63:111.Southward, A.J. (ed.), 1987. Barnacle biology. A.A. Balkema, Rotterdam, 443 pp.Steele, J.H., 1977. Some comments on plankton patches. In Spatial pattern in planktoncommunities, pp. 120. J.H. Steele (ed.), Plenum Press, New York, 470 pp.Sweeney, M.J., Roper, C.F.E., Mangold, K.M., Clarke, M.R. and Boletzky, S.V., 1992.`Larval' and juvenile cephalopods: a manual for their identication. Smithsonian InstitutionPress, Washington, USA, 282 pp.Taylor, F.J.R., 1987. The biology of dinoagellates. Botanical Monographs, vol. 27. Blackwelland University of California Press, Oxford, 786 pp.Tesch, J.J., 1946. The thecosomatous pteropods. I. The Atlantic. Dana-Report No. 28, C.A.Reitzels, Copenhagen, 82 pp.Tesch, J.J., 1948. The thecosomatous pteropods. II. The Indo-Pacic. Dana-Report No. 30,C.A. Reitzels, Copenhagen, 44 pp.Tesch, J.J., 1949. Heteropoda. Dana-Report No. 34, C.A. Reitzels, Copenhagen, 53 pp.Tesch, J.J., 1950. The Gymnosomata. II. Dana-Report No. 36, C.A. Reitzels, Copenhagen,55 pp.Thorson, G., 1946. Reproduction and larval development of Danish marine bottom inverte-brates, with special reference to the planktonic larvae in the Sound (resund). Meddelelserfra Kommissionen for Danmarks Fiskeri- og Havundersgelser, Serie Plankton, vol. 4,523 pp.Todd, C.D. and Laverack, M.S., 1991. Coastal marine zooplankton: a practical manual forstudents. Cambridg