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NOAA Technical Memorandum NMFS-F/NEC- 34

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Oceanology: Biology of the Ocean
Volume 2. Biological Productivity of the Ocean

First printed by

NAUKA PRESS

Moscow, Union of Soviet Socialist Republics

1977

Translated and reprinted by

U.S. DEPARTMENT OF COMMERCE

National Oceanic and Atmospheric Administration.

National Marine Fisheries Service

Northeast Fisheries Center

Woods Hole, Massachusetts

January 1985

NOAA TECHNICAL fCMORANDUM NMFS-F/NEC

Under the National Marine Fisheries Service's mission to "Achieve a
continued optimum utilization of liviny resources for the benefit of the
Nation," the Northeast Fisheries Center (NEFC) is responsible for planning,
developing, and managing multidisciplinary programs of basic and applied
research to: (1) better understand the living marine resources (including
marine mammals) of the Northwest Atlantic, and the environmental quality
essential for their existence and continued productivity; and (2) describe and
provide to management, industry, and the public, options for the utilization
and conservation of living marine resources and maintenance of environmental
quality which are consistent with national and regional goals and needs, and
with international commitments.

The timely need for such information by decision makers often precludes
publication in formal journals. The IHOAA Technical Memovandum NMFS-F/NEC
series provides a relatively quick and highly visible outlet for documents
prepared by NEFC authors, or similar material prepared by others for NEFC
purposes, where formal review and editorial processing are not appropriate or
feasible. However, documents within this series reflect sound professional
work and can be referenced in formal journals. Any use of trade names within
this series does not imply endorsement.

Copies of this and other NOAA Technical Memorandums are available from
the National Technical Information Service, b285 Port Royal Rd., Springfield,
VA 22161. Recent issues of NOAA Technical Memorandum NMFS-F/NEC are noted
below:

18. Stock Discrimination of Sumner Flounder (Paralichthys dentatus) in the
Middle and South Atlantic Bights: Results of a Workshop. By Michael J.
Fogarty, Glenn DeLaney, John W. Gillikin, Jr., John C. Poole, Daniel E. Ralph,
Paul (i. Scarlett, Ronal W. Smith, and Stuart J. Wilk. January 1983. iii + 14
p., 2 figs., 3 tables. NTIS Access. No. PB83-168866.

19. Environmental Benchmark Studies in Casco Bay - Portland Harbor, Maine,
April 1980. By Peter F. Larsen, Anne C. Johnson, and Lee F. Doggett. January
1983. xi + 173 p., 39 figs., 12 tables, 2 app. NTIS Access. No. PB83-184U69.

20. Annual NEMP Report on the Health of the northeast Coastal Waters of the
United States, 1981. Northeast Monitoring Program Report No. NEMP-I\/-82-65.
February 1983. xii +86 p., 21 figs., 15 tables, 1 app. NTIS Access. No.
PB83-193912.

21. MABMAP Plankton Survey Manual. By Jack W. Jossi and Robert R. Marak.
March 1983. xvii + 26U p., 41 figs., 3 tables, 2 app. NTIS Access. No. PB83-
21U203.

(continued on inside hack cover)

.^QATMOS;^,.

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NOAA Technical Memorandum NMFS-F/NEC-34

This TM series is used for documentation and timely communication of
prelimmaiy results, interim reports, or special purpose information, and
has not received complete formal review, editorial control, or detailed
editing

II

Oceanology: Biology of the Ocean
Volume 2. Biological Productivity of the Ocean

M.E. Vinogradov, Editor in Chief

Shirshov Institute of Oceanology, USSR. Academy of Sciences. Moscow. U.SS.R.

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Albert L. Peabody, Translator

Foreign Language Services Branch. National Marine Fisheries Service. Washington. DC 20235

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First printed by

NAUKA PRESS

Moscow, Union of Soviet Socialist Republics

1977

MAR»N£
BIOLOGICAL
LABORAlOftY

LIBRARY

WOODS HOLC, MASi).
\V. H. 0. I.

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0

Translated and reprinted by
U.S. DEPARTMENT OF COMMERCE

Malcolm Baldridge, Secretary

National Oceanic and AtmosDheric Administration

Anthony J Calio, Acting Administrator

National Marine Fisheries Service

William G Gordon, Assistant Administrator for Fisheries

Northeast Fisheries Center

Woods Hole, Massachusetts

January 1985

^V^NO«»^

1930

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. i !

INTRODUCTION TO THE ENGLISH EDITION

Volume 2 of the Biological Productivity of the Ocean was published
in 1977 in Russian by the Nauka Press in Moscow. The Editor-in-Chief of
the Volume is Dr. M. E. Vinogradov, Deputy Director of the Shirshov
Institute of Oceanology, USSR Academy of Sciences, Moscow. During a
USSR-USA symposium on marine ecosystems in Tallin, Estonia, USSR, parts
of the volume were discussed. Our Soviet hosts responded favorably to a
request that the entire volume be made available in an English
edition. The Office of International Fisheries of the National Marine
Fisheries Service kindly provided us with a translation of the original
Russian text. Following the initial translation the volume was
forwarded to Dr. Vinogradov for review by each of the section authors.
This English edition includes photocopies of figures from the Russian
text. In several instances they are poorly reproduced. Also, a number
of terms that represent literal translations of Russian terminology may
not be familiar to the reader. However, rather than delay the
production of the volume any further, we decided to move ahead with
distribution in its present form so as to make available to a wider
scientific audience the results of a synthesis of a considerable number
of marine ecosystem studies by Soviet scientists not otherwise readily
available in English.

The volume is divided into two parts. Part 1 deals with the
Ecology of Marine Communities, including chapters on the ecological
concepts, the structure and development of pelagic, benthic, and coral
reef communities in different global regions and from several
viewpoints, including the adaptive significance of schooling in the sea
(Chapters I, II, and III). Primary and secondary production is
discussed in Chapter IV. Part 1 concludes with a treatment of ecosystem
models in Chapter V.

Part 2 focuses on Human Activity with a discussion on the
potentials for increasing yields from fishery resources in Chapter I and
the actual and potential impacts of pollution on marine ecosystems in
Chapter II.

The Volume represents an extensive synthesis of Soviet literature
dealing with marine ecosystems which is discussed in relation to
contemporary ideas of marine ecologists in other countries. An
extensive listing of references in Russian and in English that supports
the syntheses is included.

We are indebted to our Soviet colleagues for the many hours spent
reviewing and correcting the English version of their chapters. A
special thanks is extended to Dr. M. E. Vinogradov for his willingness
to see the project through to completion following considerable

m

correspondence, including the mailings of chapters from various ports-
of-call made by research vesse.ls of the Academy of Sciences. We are
also pleased to acknowledge the cooperation of the Soviet Copyright
Agency, Moscow, for approving the translation and distribution of the
English edition. The assistance of Ms. Jurate Micuta and Ms. Prudence
Fox of the Office of International Fisheries, NMFS, Washington, for
expediting the volume and Albert Peabody for providing the initial
translation is gratefully acknowledged. Production of the volume would
not have been possible without the editorial assistance of Ms. Jennie
Dunnington who provided invaluable technical assistance in editing and
many long hours typing the entire manuscript. We are also grateful to
Ms. Elisabeth Keiffer of the University of Rhode Island for her fine
editorial assistance.

K. Sherman, English Version Editor
National Marine Fisheries Service Laboratory
Northeast Fisheries Center
iJarragansett, Rhode Island

1 V

CONTENTS

Page

INTRODUCTION TO THE ENGLISH EDITION iii

PART 1. THE ECOLOGY OF MARINE COMMUNITIES 1

Chapter I. Some Principles of the Structure and Development

of Marine Communities 1

1. General Ecologic Concepts as Applied to
Marine Communities. The Community as a
Continuum (K. N. Nesis) 1

2. The Spatial -Dynamic Aspect of Existence of
Pelagic Communities (M. E. Vinogradov) 12

2.1 Communities in Cold-Water Regions 12

2.2 Communities of the Tropical Regions 13

2.3 The Succession of a Pelagic Ecosystem 16

2.4 Changes in Structural Characteristics 18

2.5 Changes in Functional Characteristics 20

3. Nontrophic Regulatory Interactions of Marine
Invertebrates (E. A. Zelickman) 24

3.1 Metabolic Regulation 24

3.2 Pheromone Regulation 25

3.3 Interspecific Collective (Group)

Reactions 27

3.4 Intraspecific Structures of Behavior

of a Group of Individuals 31

3.5 Adaptive Value of Schooling Reactions 32

Chapter II. Pelagic Zone Communities and Their Structural

and Functional Characteristics 37

1. Trophic Relationships in the Pelagic Zone
(M. E. Vinogradov, N. V. Parin, A. G.

Timonin) 37

2. Communities of the Arctic Waters

(E. A. Zelickman) 49

2.1 Comparison of the Arctic Ecosystem

with Other Productive Systems 50

2.2 Spatial and Morphophysiol ogic Differ-
entiation of Organisms as a Form

of Transformation of Fluctuations

within the Arctic Ecosystem 51

2.3 The Seasonal course of the Process of
Production in the Arctic Community 54

Page

2.4 Perennial Changes in the Biomass of

Zooplankton of the Arctic Pelagic Zone 61

3. Communities of the Temperate Waters of the
Northern Hemisphere (S. A. Mileikovsky ,

L. A. Ponomareva, T. M. Semenova) 65

3.1 Some Biological Peculiarities of the
Planktonic Communities in the Cold-
Temperate Regions of the tJorthern

Hemi sphere 65

3.2 Planktonic Communities of the

Boreal Atlantic 68

3.3 Planktonic Communities of the

Boreal Pacific 76

4. Communities of the Temperate and Cold Waters

of the Southern Hemisphere (N. M. Voronina) 80

4.1 Phytocenes

Factors Defining the quantitative

Development of Phytoplankton 81

4.2 Zoocenes 91

4.3 Communities

Specific and Trophic Structure 103

5. Communities of the Trophical Regions of the

Ocean (A. K. Heinrich) HO

5.1 Structures of the Tropical Communities.
Specifics of Species Composition and
Boundaries between Communities.
Significance of Departing Species 112

5.2 Production Cycles 119

6. Deep-Water Communities (M. E. Vinogradov) 128

Chapter III. Benthic Communities and Their Structural and

Functional Character i sties 133

1. Littoral Communities (0. G. Kussakin) 133

1.1 Zonal ity of the Intertidal Zone 134

1.2 Factors Specific for the Littoral 136

1.3 Typology of the Intertidal Zones 139

1.4 General Characteristics of the

Littoral Biota of the World Ocean 141

1.5 Supralittoral Biota 145

1.6 Littoral Biota. Rocky Littoral Zone 146

1.7 Characteristic Peculiarities of the
Littoral Biota of the Tropics and
Circumpolar Waters 154

vi

Page
1.3 Sandy and Silty-Sandy Intertidal Zone 157

2. The ComiTiLim' ties of Coral Reefs (Yu. I.

Sorokin) 161

2.1 Reef-Building Organisms 162

2.2 Types of Coral Reefs, Their Zonal ity,
Growth and Population with Flora and

Fauna 163

2.3 Ecologic-Physiologic Peculiarities

of the Reef-Fonning Corals and Factors
Influencing Their Growth and Spread 171

2.4 Periphyton, Phytobenthos, Primary
Production and Microflora in Reef

Biotopes 177

2.5 Structure and Productivity of the

Plankton Community of Coral Reefs 179

2.6 Nutrition and Food Connections of

Reef Fauna 183

2.7 Conclusions 185

3. Fouling Communities (E. P. Turpaeva) 190

4. Benthic Shelf Communities (A. A. Neyman) 199

5. The Trophic Structure of the Benthic
Population of the Shelves (A. P. Kuznetsov,

A. A. Neyman) 204

6. Communities of Abyssal Macrofauna (Z. A.
Filatova) 212

7. Trophic Structure of the Deep-Water Benthos

(M. n. Sokolova) 218

Chapter IV. Production of Marine Communities 228

1. Primary Production (0. I. Kobl entz-I'li shke,

V. I. Vedernikov) 228

1.1 Methodologic Problems 229

1.2 Comparison of Results of Determination
of Parameters of Primary Production

at the Surface of the Ocean 233

1.3 Environmental Factors Influencing

Primary Production 237

2. Production of Microflora (Yu. I. Sorokin) 256

2.1 Methodologic Problems 256

VI 1

Page

2.2 Number, Biomass and Production of
Planktonic Microflora in Communities

with Various Levels of Productivity 260

2.3 Microflora of the Bottom Sediments 264

2.4 Microflora of Detritus of

Peri phy tonic Foul ing 266

2.5 Biogeochemical Activity of Marine
Microflora 256

2.6 Intensity of Microbial Decomposition of
Organic Matter and Consumption of

Oxygen in the Water and in Sediments 267

2.7 Participation of Microorganisms in the
Cycling of i^utrients 273

2.8 Significance of Microbial Biosynthesis

in the Cycle of Some Mineral Elements 275

2.9 The Trophic Role of Microflora in

Marine Ecosystems 277

3. Production of Zooplankton (E. A. Sushkina) 286

3.1 Methods of Calculation of the
Secondary Production and Ecologic-
Physiological Characteristics of

Planktonic Animals 288

3.2 Methods of Calculation of the

Production of Communities 295

3.3 Estimate of Production of Populations,
Trophic Levels, Zooplankton and the
Planktonic Community as a Whole 298

4. Production of Zoobenthos (A. Nl. Golikov,

0. A. Scarlato) 304

Chapter V. Mathematical Modelling of the Functioning of a

Pelagic Ecosystem 320

1. Simulations of the Functioning of a
Pelagic Ecosystem (M. E. Vinogradov,

V. V. Menshutkin) 322

1.1 Statement of the task of Modelling of
Balance Relationships in Oceanic Pelagic
Ecosystems 322

1.2 Model Considering Distribution of

Elements of an Ecosystem with Depth 324

1.3 Model Considering the Distribution of
Elements by Area 334

1.4 Model Simulating the Volumetric
Distribution of Elements ...339

2. Stochastic Models of Communities (B. S.
Fleishman) 342

VI 1 1

Page

2.1 Dynamic Model of Communities Ignoring
Aggregati on 343

2.2 Model Study of Optimal Strategies of
Community 347

2.3 Static Model of Community Considering
Aggregation 355

PART 2. HUMAN ACTIVITY AND THE BIOLOGY OF THE OCEAN 359

Chapter I. Biological Resources of the Ocean and

Possibilities for Increasing Them 359

1. Fishery Production of the World Ocean and

Its Utilization (P. A. Moiseev) 359

1.1 Productive Regions of the Ocean 361

1.2 The Level of the Modern Catch 364

1.3 Regional Placement of Marine Fishery 380

1.4 Basic Trends in Future Development

of Ocean Fishery 393

2. Introduction and Acclimatization of Marine
Organisms (T. S. Rass, 0. 6. Reznichenko) 396

2.1 Factors and Phases of Acclimatization 397

2.2 Forms of Acclimatization 398

2.3 Transoceanic and Inter-Oceanic Trans-
pi antati on 399

2.4 Parameters of Introduction and

Accl imatization of Exota 404

Chapter II. Effect of Ocean Pollution on Marine Organisms

and Communities 406

1. Chemical Pollution and Its Effect on
Hydrobionts (S. A. Patin) 406

1.1 Status and Methodology of Investigations 406

1.2 Basic Features and Trends in Pollution

of Ecologic Zones of the World Ocean 408

1.3 Biologic and Ecologic Effects of

Pol 1 uti on 414

2. Accumulation of Radionuclides by Hydrobionts

and Its Results (G. G. Polikarpov) 418

3. Anthropogenic Thermal Effects on the

Population of the Sea (S. A. Mileikovsky) 421

IX

Page

3.1 Amount of Thermal Pollution of Marine
Coastal and Estuarine Waters, Temperature
of Waters Dumped and Changes in
Temperature of Natural Waters which

Resul t 421

3.2 Influence of Thermal Pollution on the
conditions of Existence of Flora

and Fauna 422

3.3 Influence of Thermal Pollution on the
Distribution of Flora and Fauna 423

3.4 Passage of Pelagic Fish through the
Pipes of Plants and Industrial

Enterprises 424

3.5 Change in the Pacific Composition of
Communities in Regions of Thermal

Discharge 425

3.6 Influence of Thermal Discharge on the
Biology of Organisms 425

3.7 Degree of Harm of Thermal Pollution

of Marine Coastal and Estuarine Waters 426

RUSSIAN REFERENCES 428

REFERENCES IN OTHER LANGUAGES 471

PART I. THE ECOLOGY OF MARINE COMMUNITIES

CHAPTER I. SOME PRINCIPLES OF THE STRUCTURE AND DEVELOPMENT

OF MARINE COMMUNITIES

1 . General Ecologic Concepts as Applied to Marine Communities.
The Community as a Continuum. (K. N. Nesis)

The concept of the "biocenosis" was introduced by Mobius (1877).
Mdbius defined a biocenosis as a community of organisms inhabiting an
individual area of the environment; the composition and quantitative
relationships of the species of a community correspond to the mean of
the extremes of the environmental conditions. The members of the biocenosis,
according to Mobius, directly or indirectly depend on each other and
mutually serve each other so that a self-regulating biologic equilibrium
is formed, fluctuating about its mean position (Hesse, 1924). This
definition emphasizes first of all the biologic interconnection and inter-
dependence of the organisms of the community. This concept, introduced by
Mdbius, is firmly rooted in ecology.

The most important stage in the development of marine ecology was the
introduction of a quantitative method of investigation of the benthos and
bottom communities, connected with the name of Petersen (1911-1918).
Petersen, however, had a quite different understanding of the word community
than did Mobius. Communities, according to Petersen, were statistical units,
regularly repeated groups of species encountered together, recognized (and
named) after the most numerous and characteristic species which "struck the
eye." The studies of Petersen were quite fruitful and stimulated extensive
development of research in the area of quantitative accounting for the
benthos (Zenkevich, 1947, 1963). The term "Petersen communities" has been
firmly implanted in the ecologic literature.

However, at the same time, a Mdbius concept of the community as a group
of ecologically related organisms continued to exist and develop. The view
of the community as a structure with such close and numerous internal
connections that it could be likened to human society or even a super-
organism developed. "Animal communities . . . are not mere assemblages of
species living together, but form closely knit communities or societies
comparable to our own," wrote one of the founders of modern ecology, C.
Elton (1927, p. 5). Naturally, for the proponents of this view, the
Petersen concept of the community was unacceptable. As a result of the
extended discussions of the 1920s and 1930s, two concepts were developed in
ecology, particularly in hydrobiology : communities of animals are
statistical units, and communities are biologic units (Thorson, 1957). The

1

views of the proponents of the biologic concept are well reflected by
the words of D. N. Kashkarov: "The word biocenosis is constantly
applied to widely varied groups of organisms, without the slightest
attempt to understand the connections between them, to understand the
internal relationships in the biocenosis. ... In this sense hydrobiolo-
gists are great offenders. Any isolated accumulation of various organisms
is immediately referred to as a biocenosis. . . . The result is a
purely formal . . . and therefore fruitless description of phenomena"
(1938, p. 271).

The concept of the biocenosis as a super-organism (Thienemann, 1925:
Clements, Shelford, 1939; etc.) has been severely criticized. Particularly
important has been the criticism from those who look upon a community as
a continuum. The view of a community as a group of unrelated species, which
react similarly to environmental conditions and are distributed along a
gradient of environmental factors in accordance with the degree of tolerance
of each species, agrees well with the concept of the community as a
statistical unit, but is incompatible with the biologic concept of the
community.

The development of the biologic concept of the community was greatly
influenced by the development of such concepts as the trophic level, food
chain and stages of succession (Elton, 1927, 1934; Kashkarov, 1938, 1945;
and others). A new step on this path was the combination of the dynamic
aspect of community (succession) with the views of V. I. Vernadsky concerning
the biogeochemical role of living matter and the development of the tropho-
dynamic concept of ecology on this basis (Lindeman, 1942). The trophodynamic
aspect of the study of aquatic ecosystems developed rapidly, leading to the
development of the theory of food chains (Riley, 1963a), the quantitative
theory of biological productivity of the sea (Gushing, 1959a), the intro-
duction to hydrobiology of cybernetic concepts (Margalef, 1956, 1968;
Patten, 1959, 1966), and the development of mathematical models of
aquatic ecosystems (Riley, 1963; Gushing, 1959a; Vinberg, Anisimov,
1966: Lyapunov. 1971; Menshutkin, 1971; Vinogradov et al . , 1971; Odum,
1975, etc.).

The study of the structure of aquatic communities has also led to
extremely important conclusions. It has been found that the composition
and relations of species in a biocenosis is not unambigiously determined
by the peculiarities and mosaic of external conditions (the biotope). The
leading species of common benthic biocenoses are selected according to the
principle of the least competitive interactions (Ivlev, 1954; Shorygin,
1955). If we rank the leading species of a biocenosis in order of mean
biomasses, the neighboring species in the series thus produced will
generally belong to different trophic groups (Turpaeva, 1949, 1957; A. P.
Kuznetsov, I960), and if they are in the same trophic group, they usually
belong to different zoogeographic groups (Neyman, 1963a, 1967). This
rule, first determined empirically and later confirmed with extensive
factual materials, has provided an important confirmation of the value of
the Petersen concept of benthic communities.

Thus, in marine biology, two different views on marine communities
have developed; more precisely, two models of marine communities have

been created. The first model, widely used in planktonology, is based on
the trophodynamic aspect of an ecosystem ("the Lindeman approach"). It
looks upon a community as a system of organisms at various trophic levels,
related primarily by predator-prey relationships, i.e., "strong relation-
ships"--by analogy with physical phenomena in the microcosm (MacArthur,
1972). This aspect of a community is the basis of many models of eco-
systems, beginning with the classic approach of Lotka and Volterra and
extending to quite modern works.

The second model, more widespread among researchers studying benthic
fauna, concentrates attention on the organisms of a single trophic level
and their interactions. For simplicity, it is assumed that migrating
organisms are not included in the biocenosis (Thorson, 1957; and others).
This means that predators which enter a given biocenosis only to feed are
practically not studied. If we consider that most of the floor of the
seas and oceans lies below the zone of habitation of producers, it can
be stated that a typical benthic biocenosis is populated primarily by
consumers of detritus.

The interrelationship of species in both models, naturally, is
studied on the basis of the same primary postulates of ecologic science--
Elton's theory of the ecologic niche and the law of competitive exclusion
of Volterra and Gause. The stability of the "vertical" model requires
maximization and stabilization of relationships between species, since
these species are of different trophic levels, while stability of the
"horizontal" model requires minimization of species relationships, i.e.,
the greatest possible separation of niches.

The most important processes in marine biology in recent years have
been related to reconsideration of these traditional models of ecosystems.
In planktonology, works have been extensively developed on the study of
"nonpredatory" ecologic relationships, primarily the interrelationships
between organisms mediated by external metabolites (Johnston, 1955; Lucas,
1955, 1965; Provasoli, 1958; and many others), developing in the study of
the ecologic metabolism of the sea (Khaylov, 1971). It has become clear
that exocrines and dissolved organic matter bind the producers, consumers,
predators and reducers into a single network, which corresponds more
closely to the actual picture of a conmunity than a network based only
on trophic relationships. The role of external metabolites is varied: They
act as food (dissolved organic matter), sources of indispensable substances
(vitamins, particularly Bi2» trace elements, vital amino acids), as sub-
stances which suppress the growth of competing organisms, as signalling
substances, etc. Consideration of this type of relationships between
species can answer many curious questions in the ecology of marine communi-
ties. For example, the differing demand for external metabolites such as
growth substances and vitamins, the capability of a species to grow with a
lower concentration of these substances, may be one of the factors involved
in specialization of species of phytoplankton and one explanation of the
"plankton paradox" (Hutchinson, 1961)--the coexistence of phytoplankton
species with similar demands for the primary biogenes, which should,
therefore, be in acute competition. Furthermore, if any organism requires

a vital substance which it cannot obtain from sea water, it will be forced
to consume sufficient food to satisfy the demand for this substance (the
Liebig minimum law). If the minimum quantity of food necessary to
satisfy the demand for the limiting substance is significantly greater than
that quantity of food necessary to satisfy the energy demands of the
organism, it will be energetically favorable to the organism to convert
the food only to the stage at which the radicals and active centers required
by the organism are split off, and then to excrete the remainder in minimally
converted form. The ecologic effectiveness of a population in this case
will be significantly lower than the calculated effectiveness based on
metabolic, growth and generative demands alone, and the excretions can serve
as food for other animals, particularly for DOM consumers.

The view on the benthic biocenosis as a community of independent
organisms, equally reacting to the abiotic conditions of the environment,
has been significantly modified by the acknowledgment of the tremendous,
decisive role of biologic, or more precisely symphsiologic (V. N. Beklemishev,
1951) interrelationships in marine communities (reviews: Miloslavskaya,
1961, 1964). Minimization of the competitive interrelationships between
species is a statistical, climactic aspect of the community; in the dynamic,
successional aspect, we see the entire variety of inter- and intra-speci^s
interrelationships: when competition between two (or more) species modifies
the reaction of these species to abiotic conditions, when the relationships
of two (or more) species are modified by the influence of a third, etc.
For example, the acorn barnacles Chthamalus stellatus can flourish throughout
the entire intertidal area, but cannot withstand the competition of Balanus
balanoides. As a result, they form a belt in the uppermost shore
horizon, where the Balanuses cannot exist due to the severe environmental
conditions. For the Balanuses , as for the Chthamaluses , the habitat
conditions are better the lower the level at which they live. However,
in the lower intertidal zone the dog-whelks Nucella lapillus, the principal
enemy of the acorn barnacles, are numerous. Therefore, balanuses of all
ages inhabit the upper level of the intertidal zone, while the lower level
is inhabited only by large individuals, too large for Nucella. The exis-
tence of these three species is possible due to their varying tolerance to
the stress conditions in the upper tidal levels, but their distribution in
belts does not reflect the distribution of the optimal conditions for their
existence at all (Connell, 1961a, b). The alga Hedophyllum sessile
finds its optimal conditions of existence in the surf zone, but is numerous
there only in areas with moderate wave action, since in heavy surf it cannot
withstand the competition of Laminaria setchelli and Lessoniopsis littoral is.
The sea urchins Strongylocentrotus purpuratus devour these algae and may
consume them completely, thus liberating the place for Hedophyllum. If an
area of the bottom is cleared from the sea urchins, then Laminaria and
Lessoniopsis rapidly crowd out Hedophyllum and its associated algae (Dayton,
1975) . Studies of this type of interrelationship between species have led
to the development of the concept of "key species" in a biocenosis, the
ecologic influence of which significantly exceeds their part in the number
and biomass of the biocenosis. Usually, the key species is a predator,
occupying a high position in the food pyramid of the biocenosis and
consuming, selectively or nonselectively, organisms which, were it not for

the restraining influence of the predator, could monopolize the space
or food resources and thus squeeze out less competitive species. For
example, the starfish Pisaster ochraceus feeds primarily on mussels. When
these starfish are absent, the mussels are the masters of the tidal zone,
squeezing out the balanuses and other animals and greatly reducing the
species variety (Dayton, 1971; Fotheringham, 1974; Menge, 1972; Paine,
1966, 1969a, b, 1974). In exactly the same way, the starfish Pycnopodia
hel ianthoides holds down the number of the urchins Strongylocentrotus spp.--
macrophyte feeders (Mauzey and other, 1968). In the opinion of Payne (1966),
the local species diversity is directly related to the effectiveness with
which predators prevent monopolization of the primary necessary resources by
a single dominant species. The number and biomass of such key predators
are low--they also have a vulnerable link in their life cycle. This is
usually so for the pelagic larvae or fry. In particular, one important
limiting aspect in the life of the predator might be the heterogeneous
and, consequently, unpredictable for the predator, distribution of the
food on which the young animals feed (Birkeland, 1974).

The formation and existence of climax communities are possible only
under stable environmental conditions, in which changes are predictable
in terms of period, phase, and amplitude, and do not go beyond the limits
of tolerance of the organisms. If the changes are sharp and unpredictable,
the climax community is disintegrated or disrupted. The places which are
liberated are occupied first by opportunistic species, characterized by
rapid reproduction, early maturation, high fertility, short life cycle,
high mortality, and simple population structure (Pianka, 1970, 1972).
During the course of the succession, they are gradually replaced by more
competitive dominant species. In permanently unstable biotopes, a climax
is not established and opportunistic species predominate permanently.
However, even in stable communities, they may exist, due to aperiodic (and
therefore unpredictable) disruptions in the structure of the community,
forcibly throwing it into the initial stages of succession. On the land,
these disruptions are caused by forest fires, floods and other factors;
at sea--by hurricanes, tsunamis, earthquakes, outbursts of predators, etc.
Thus, during the past decade on the coral reefs of the Indo-West Pacific
area (Great Barrier Reef, Guam, etc.), an unprecedented burst in the
development of the "crown-of-thorn" starfish Acanthaster placi has been
observed (Chesher, 1969; Pearson, Endean, 1969; and many others). The
coral reefs of the Indo-West Pacific are among the most mature and stable
of all ecosystems in shallow waters of the world ocean. Acanthaster is
usually an extremely rare animal (a few individuals per square kilometer),
with old individuals predominating in the population. The mature starfish
feed exclusively on hermatypic corals, and the substances excreted as the
starfish feed on the coral attract other starfishes. In cases of massive
multiplication, this property may lead to the formation of accumulations
of many starfish in small areas of reef damage, frequently hundreds of
individuals. The starfish attack the coral and destroy it almost completely,
and all of the fauna associated with the living coral die. On the surface
of the dead coral, algae develop immediately, followed by soft corals, etc.
This same succession is observed during restoration of a reef destroyed by
an earthquake (D. V. Naumov, personal communication). Complete restoration

of the disrupted community requires many years or even decades. It is not
yet clear whether massive development of Acanthaster occurs periodically,
or whether this is an unprecedented phenomenon, related to anthropogenic
influence on the community (Endean, 1973). This sort of disruption of a
mature community plays a significant role in the evolution of the reefs,
creating a temporary mosaic of various stages of succession and allowing
the existence of opportunistic and fugitive species (Grassle, 1973).

Human activity has the same sort of influence on a community. Oppor-
tunistic species occupy the primary position in the list of organisms
indicating pollution. They are the lest to disappear when pollution becomes
fatal for all life, and the first to appear in the course of self-purification
(Grassle, Grassle, 1974). Man's influence may also cause brief disruption
of mature communities. For example, on the shores of Puget Sound
(Washington), the climax community consists of ubiquitous colonies of
mussels. During stormy weather, the mussels die due to the impacts of
logs lost in timber floatage, which strike the rocks quite forcefully.
The empty spaces thus formed are rapidly covered with a bacterial -algal
film, after which these spots are inhabited by Chthalamus dall i , followed by
Balanus glandula , then B. cariosus and finally young mussels which,
with time, completely displace the algae, as well as the limpets, which
feed on them, barnacles, etc. (Dayton, 1971; Payne, 1974).

The activity of "key species" can come to the same process--preventing
full colonization of a space and of all available food resources by dominant
species and exclusion of opportunistic species, except that they do this
constantly and gradually, not catastrophical ly rapidly.

Studies of such processes have established the extremely important
role of the indirect, "weak" (MacArthur, 1972) relationships between
species, which may change the tolerance of species to abiotic and biotic
environmental factors and shift the equilibrium of the direct relationships
(Turpaeva, 1969, 1972; Turpaeva, Maksimov, 1971; Darnell, 1970; Dayton,
1971 ; and others) .

The idea of the selection of communities from species which interact
minimally with each other has been applied in works dedicated to the
analysis of the structure of plankton ecosystems. In studying the phyto-
plankton of Pamlico Sound (North Carolina), Hulburt and Horton (1973) stated
the hypothesis that conditions favoring the creation of a high biomass
of phytoplankton might be dual: In one case, the growth of phytoplankton
as a whole is accelerated, while in another, the interactions between
species are minimized. In this latter case, one might observe either a
stop in the growth of one species, allowing rapid multiplication of another,
usually competing, species, or both species, multiplying rapidly and
simultaneously, no longer hindering each other or, finally, the development
of one species begins after the other, but their maxima overlap. The
conditions of minimization of interaction, therefore, are manifested in
that the influence of the law of competitive exclusion of species occupying
the same niche, limiting the growth of the biomass, is removed; the "either-
or" principle (either one species or another with which it competes) is
replaced by the "and" principle.

However, in plankton communities, the possibility of dispersion of
species into different ecological niches is in principle less than in
benthic communities. Divergence as to type of substrate, of course, is
impossible, as to synusia--quite difficult; the basis of specialization
becomes differentiation as to the nature of food, time and conditions of
feeding and seasons of development. Therefore, in plankton communities,
the significance of weak interactions and the factors minimizing the
interrelationships are probably significantly less important than in
benthic communities.

In recent times, since the development of the modern concept of the
biological niche--the "Hutchinson niche" (Hutchinson, 1957, 1959), the
concept of stability of ecosystems and the relation of stability to
processes of succession (MacArthur, 1955; Margalef, 1963a, b, 1968), the
concept of packing density of niches (MacArthur, 1960, 1965) and the
creation of the "stability-time" hypothesis (Sanders, 1968. 1969;
Slobodkin, Sanders, 1969; Grassle, Sanders, 1973), it has become possible
to consider two seemingly mutually exclusive concepts of the biocenosis--
the statistical and biological ones--as two sides of a single coin. It
can be thought that the biologic concept of the biocenosis analyzes the
dynamics of the process of development of the architectonics (structure)
of the community, while the statistical concept studies the result of this
process, i.e., the structure of the climax community. In discussing the
question of the structure of a community, we silently assume that the
wery concept "community = biocenosis" is unambiguously understood and
reflects the actual natural phenomenon. However, this is far from completely
accepted.

First of all, the concept of the community as an undivided unity of
plant and animal organisms is widespread in ecology (V, H. Beklemishev,
1928; Kashkarov, 1933), as is the concept of the biocenosis as a union of
organisms capable of independent existence (Allee and others, 1949). Many
authors use the term biocenosis to refer only to a self-sustaining, ener-
getically autonomous "large community," including producers, consumers and
reducers (see Za'fka, 1967), From this standpoint, the Mobius biocenosis is
not a biocenosis at all, but only a dependent or incomplete community; the
population of an oyster bank, for which the term was first suggested,
includes almost no producers and exists primarily on the organic matter
(detritus) which is produced in other communities. If we strictly follow
this point of view, we cannot apply the concept of the biocenosis to the
benthos of zones below the lower boundary of the phytal area, in other
words to the population of spaces covering more than 2/3 of the surface of
the Earth; this concept is then also inapplicable to the fauna of the
bathypelagic and abyssopelagic zones, as well as the oligotrophic areas of
the pelagic zones in the tropical oceans. In other words, if trophic
completeness and functional independence are considered necessary charac-
teristics of a biocenosis, we must state that there is but one biocenosis
on Earth--the Geomeride. It seems more correct to consider a community in
its initial Mobius significance as a set of living organisms within the
limits of a homogeneous biotope. A biocenosis may include either organisms
of all trophic levels, or only consumers.

The constancy of the composition of a community and the distinctness
of the boundaries between neighboring communities existing in the environ-
ment, which has no such constancy or clear boundaries, is possible, as
V. N. Beklemishev (1928) emphasizes, only if there is some internal organi-
zational factor, due to which certain combinations of organisms are
stable, while those intermediate between them are unstable, even if they
live under intermediate conditions. The existence of such a factor,
however, is hardly axiomatic. There is another point of view, first stated
in 1910 by the geobotanist L. G. Ramensky: Vegetation is a continuous whole.
The species are autonomous and have no organic relationship with each other.
Species which respond in the same way to certain environmental conditions
inhabit the same area, but, due to the ecologic individuality of each species,
the boundaries of the ranges of various species do not coincide, so that
the groups of species merge smoothly with each other. There are no com-
munities; there are only coinciding species within the limits of the continuum,
This concept has become widespread in geobotanics since the late 1920s, and
has extended into marine biocenology.

The concept of the marine benthic community as a continuum has been
developed primarily by A. Lindroth (1935, 1973). In his opinion, the
concepts of trophic levels and trophic connections should be applied not
so much to individual species as to life forms. The distribution of species
in communities depends primarily not on species-specific relationships
between them, but rather on their relationships to environmental factors
which they all encounter. A sharp gradient in the environmental factors
represents a boundary for the extension of many species in the community
simultaneously. If the gradient is not great, the species are distributed
along the gradient independently of each other, so that a continual
distribution develops. The boundaries of a community are not clearly
outlined, communities merging one into another. The boundary of distribution
of the ecologically dominant species is, naturally, the boundary for the
fauna and flora associated with it as well. Lindroth (1973) suggests that
homogeneous communities be called coenotypes, that communities with gradually
changing composition be called coenocl ines. Among the coenotypes, he
distinguishes abiogenic coenotypes, limited by sharp gradients in abiotic
conditions; biogenic coenotypes, related to changes in ecologic dominants;
and plateau coenotypes, homogeneous communities with unclear clinal-type
boundaries.

A typical example of a coenocline, according to Lindroth (1935), is the
community of soft, silty bottoms. The composition of this community results
from external factors. Definite and rather individualized communities may
be encountered wherever a dominant species of organism develops, i.e.,
wherever the coenocline becomes a biogenic coenotype. In the opinion of
Lindroth, based on the study of the benthos of Gullmar Fjord (western
Sweden), it is quite impossible to distinguish associations for such
regions, since the "colonies" gradually merge with each other, with no sharp
boundaries. Many other researchers studying the benthos of soft bottoms have
reached similar conclusions (Vorob'yev, 1949; Lie, 1968a, 1969, 1974;
Lie, Kelley, 1970; Lie, Kisker, 1970).

8

A second example of an analogous structure of a community is to be
found in the benthic communities of the intertidal and phytal zones.
BoudouresQue (1971a) demonstrated that the species composition of algae
in the Mediterranean sea near Marseille changes continually with depth,
the distribution of each species of algae changing along a transect
independently of the others, although in some places there is a sudden
change in species composition. A similar conclusion was reached by 0. G.
Kussakin et al . (197^, p. 23). At times, the fauna is distributed
less discretely than the flora (Denisov, 1974; Boudouresque, 1971a, b).
Of course, such cases--and the number of examples may be quite great--
fit well into the system of Lindroth.

The empirical conclusions of Lindroth were subjected to theoretical
analysis by Fager (1963), Mills (1959), G. F. Jones (1969), Boudouresque
(1971a) and other authors (see the reviews of Longhurst, 1964, and
W. Stephenson, 1973). It follows from these works that the species of
animals and plants, both in the water, and on the bottom, are distributed
so that each of them reacts to gradients of environmental factors independ-
ently of the others. The environmental factors may be abiotic or biotic,
the latter including most commonly the influence of the dominant species,
the edifier species. Communities of species are, strictly speaking,
recurrent groups, i.e., groups of species which usually (in the statistical
sense of the word) are encountered together. This simultaneous encountering
of members of the group results from the similarity of their response to
environmental factors. Under conditions of extreme variability of abiotic
environmental factors, these factors may have a decisive influence on the
composition of a community--such biotopes are occupied by "physically
controlled communities." As the variability of the physical (abiotic)
factors decreases, biotic relationships take over, and in biotopes with
relatively stable abiotic conditions, "biologically accommodated" or
"biologically fitted" communities arise. They differ from physically
controlled communities in that the former are composed of species which
react identically to certain gradients in abiotic conditions, while the
latter consist of species which are "fitted" to each other, mutually
adapted to coexistence. Thus, a community can be defined as a "group of
organisms occurring in a particular environment, presumably interacting
with each other and with the environment, and separable by means of
ecological survey from other groups" (Mills, 1969, p. 1427). Each community
is, therefore, a "relative continuum between relative discontinuities"
(Boudouresque, 1971a, p. 132). To describe communities of this type,
Boudouresque (1971b) used the concept of the nodum. A nodum is an
accumulation ("constellation") of points in a certain hyperspace, completely
or partially isolated from other such accumulations. Groups of species
which react identically to environmental factors are nodes within the
multidimensional continuum. A community is also a nodum, i.e., a sector
of the continuum limited by a space of interrupted continuum, an ecotone.
A biocenosis (parallel to a community in the sense of Thorson) is a nodum
consisting of a certain number of elementary nodes--ecologic or recurrent
groups.

It is not difficult to see that the concept of the community as a
continuum limited by sectors of interrupted continuity corresponds best to
the model of the biocenosis as a structure with negative interspecific
correlations, i.e., with the least competitive interactions (Ivlev, 1954;

Shorygin, 1955: Turpaeva, 1949, 1957). Shorygin's "sharp-topped" bio-
cenosis, i.e., a community with sharp domination of one species (or life
form), will correspond in this case to the community of an edifier species
or the biogenic coenotype of Lindroth,* while the "flat-topped biocenosis,"
without sharp domination of one species (or life form) will correspond
to the abiogenic or plateau coenotype, i.e., a community of independent
species.

The direct practical application of the concept just described is
related to the identification of the boundaries of communities. This
question has been greatly discussed in the literature (see Odum, 1975,
Chapter 6, paragraph 3). It has been the practice of domestic specialists
in the study of benthic fauna to make wide use of the principle of separa-
tion of biocenoses by the dominant (in biomass) species in a given sample
or group of samples taken at the same or neighboring stations (Vorob'yev,
1949; Neyman, 19638). If we accept the concept of the community as a
continuum, it becomes impossible to distinguish communities on the basis
of this characteristic. This would be impossible, even when the equipment
usually used in expeditions for quantitative sampling could give us a
completely adequate idea of the biomass of each species, which is not the
case. At the present time, it is most frequently recommended that com-
munities be differentiated by using the method of distinguishing recurrent
groups (Fager, 1957, 1963; Fager, McGowan, 1963) and various variants of
multidimensional analysis.

The initial question in the problem of the community as a continuum--
the existence or nonexistence of an internal organizational factor--can
now in principle be considered answered, since it has been demonstrated
(Patten, 1961c, 1952, etc.) that the stability of a community of organisms
is greater than the stability of their environment. Natural communities
evolve, adapting their structure to the environmental conditions and
optimizing their species composition and interspecific quantitative
relationships. Maintenance of a stable structure of the community requires
certain expenditures of energy, defined by the flow of negentropy (Patten,
1961a). The community reacts to environmental conditions in such a way as
to create a structure allowing the greatest energy yield ("income") given
the available distribution of resources. Therefore, communities which pay
the lowest price (measured in units of negentropy) to maintain the
corresponding structure receive a selective advantage (Patten, 1961b, 1953),
Thus, certain states of communities of organisms are truly more stable than
others, even with intermediate values of abiotic environmental factors.

*In the limiting case, a biogenic coenotype consists of a community
consisting of an edifier species and species directly related to it. This
type of community is a consortium, which geobotanists define as a combination
of dissimilar organisms closely related to a productive organism or popula-
tion (core of the consortium) and with each other in their vital activity.
An oyster bank is an example of a consortium.

10

The evolution of ecosystems as a process of increasing their degree of
self-organization is now an established fact (Dunbar, 1960, 1972; Patten,
1966; Margalef, 1968). However, this does not negate the possibility
of the existence of groups consisting of independent or weakly dependent
species, which merge smoothly together. The evolution of communities may
follow the path of increasing interconnections between organisms, or
of minimizing interspecific relationships. In either case, however, the
biocenotic levels of organization are less integrated, less individualized
and less isolated than the organismic and population levels. As V. N.
Beklemishev (1964) put it, the boundaries between communities are no less
indefinite and difficult to see, but also no less real, than the boundaries
between atmospheric or oceanic currents. From this it follows that the
concept of the community as a continuum is quite applicable for analysis
of a number of specific biocenotic situations and should take its place in
the methodologic arsenal of marine biology.

11

2. The Spatial-Dynamic Aspect of Existence of Pelagic Communities
(M. E. Vinogradov)

Due to the mobility of the biotope, the water, pelagic communities
differ significantly in their structural and functional characteristics
from other marine communities, and the analysis of their development from
this standpoint is of particular interest.

In the volume on "The Biologic Structure of the Ocean," in the chapters
dedicated to the bioqeography of pelagic animals and their distribution, it
was stated that the bases of the areas of distribution of most species in
the pelagic zone are related to quasi-steady circulation of the waters,
usually including not only horizontal motion, but also vertical motion. The
circulation may have various dimensions and various degrees of "openness."
Sometimes, preservation in the circulation of but an insignificant portion
of a population supports reproduction and the existence of the species
with its area of distribution, even though most of the population is scattered
and unproductively lost.

The great oceanic or shoreline circulations form the basis for the area
of distribution of many planktonic species which, together with species
transported from other circulating currents or entering a given circulation
for a time as a result of vertical and horizontal (nektonic forms)
migrations, make up the community of a given region.

The biotope of a community--the aquatic medium--is continually renewed,
while its characteristics change regularly as a result of seasonal or
hydrodynamic factors. The community populating the water also undergoes
regular changes.

2.1 Communities in Cold-Water Regions

In regions with a clearly expressed seasonal cycle, changes are
determined primarily by this cycle. They will be analyzed in greater
detail in Chapter II, paragraphs 2-4; here, we will briefly discuss certain
aspects, in order to show that the development of pelagic communities of
cold-water and tropical regions of the ocean follows, on the whole, the
same regularities.

In temperate and cold-water regions, the enrichment of the surface,
euphotic layers with nutrient salts occurs primarily due to winter convection
extending into the layer beneath the euphotic zone, where the concentration
of nutrients is high throughout the year. The winter minimum in the
development of phytoplankton is followed by the spring pulse, resulting
from the increase in the intensity of solar radiation and, no less signifi-
cantly, the development of stable stratification of the water above the
basic pycnocline.

When the seasonal pycnocline develops, the bloom of phytoplankton may
sometimes even begin beneath the ice (Konovalova, 1972), whereas in the

12

spring, if insolation is sufficient, but stratification is not stable,
the phytocenosis is subject to such great losses--transport of cells from
the euphotic zone by turbulent mixing--that the avalanche-like bloom of
phytoplankton does not occur.

Soon after the peak of the pulse, the phytoplankton begins to die,
the water becomes rich in suspended and dissolved organic matter, which
serves as the basis for the development of masses of bacteria and protozoa--
the heterotrophic flagellata and infusoria (Sorokin, 1974; Pasternak,
Shushkina, 1973). It is this "protonutriment" in the surface layers above
the thermocline which serves as the food base for most of the herbivorous
plankton, the quantity of which tends to increase rapidly, reaching its
maximum 1-3 months after the beginning of the bloom. The biomass of the
predators reaches its maximum later, and their pressure on the herbivorous
plankton differs in different regions and, apparently, experiences signifi-
cant annual fluctuations.

The developing community changes not only with time, but also,
following the currents, moves in space. Since stratification (the develop-
ment of the seasonal thermocline) may not occur simultaneously in different
regions, even though they be close together, the communities in different
areas in the moving water may be in different stages of maturity later on.
However, these differences, even over large regions, are generally not
great, so that the beginning of the spring pulse, over the great, hydrologi-
cally homogeneous areas of water, fluctuates within a narrow interval of
time. The intensity of consumption of phytoplankton by zooplankton, even
within the limits of a single zone or a single community, is also not uniform
over the entire water area (Heynrih, 1957; Kashkin, 1962; Kamshilov et al . ,
1958; and others). As a result, the picture of distribution of plankton is
always rather variegated in both the space and the seasonal respects.

2.2 Communities of the Tropical Regions

In the tropics, where seasonal cooling of the surface water is slight
or nonexistent, winter convection does not occur. Enrichment of the surface
layers with nutrients occurs primarily in areas of quasi-steady upwelling of
water, caused by hydrodynamic factors (zones of divergence of currents,
upwelling of water near the shores of continents, resulting from onshore
winds, the influence of islands and underwater banks). Studies performed
on special cruises of the VITYAZ have allowed us to construct a schematic
diagram of the circulation of nutrients in the ecosystem of the active
layer of the pelagic zone of the tropic ocean, which determines the picture
of development of its community (Vinogradov et al . , 1971).

In a zone where the water ascends, the pycnocline is close to the
surface, nutrients penetrate into the surface layer, and development of
phytoplankton begins in this layer. The water flows outward from the
upwelling zone. Temperature (density) stratification of the layers of
water becomes more precise, intermixing decreases and the upper boundary of
the thermocline descends. Nevertheless, nutrients, as a result of turbulent
intermixing, continue to reach the upper, mixed layer, from below, though in
decreasing quantities (Fig. 1). This flux of nutrients from below is

13

^ Divergence (upwelling)

0

Convergence

too

m-\ -»

Fig. 1. Diagram of turnover
(DOM) in the succession of a
ocean. Top: 1, Ascent of nu
utilization in the cycle of p
community; 3, Loss of nutrien
organisms; 4, Turbulent risin
the lower maximum of phytopla
DOM rising from the lower max
surface community. Bottom:
of phytoplankton at various d
and bottom phytoplankton maxi

of nutrients and dissolved organic matter
pelagic community in the tropic waters of the
trients and DOM in upwelling; 2, Repeated
roduction and destruction of the surface
ts with descending organic residue and migrating
g of nutrients and DOM and their retention at
nkton and bacteria; 5, Intake of nutrients and
imum layer into the productive cycle of the
Variation in distribution of relative quantity
istances from the upwelling zone (a, b, top
ma) (Vinogradov et al . , 1971).

consumed by colonies of phytoplankton and bacteria formed in the layer
above the thermocline, which serves as the dividing line between the portion
of the community which lives above it and the source of nutrients below.

The population of the layers above the underlying maximum exists
primarily on the nutrient salts transported by the flow of water from the
ascending zone to the descending zone. These nutrients, entering the cycle
of production and destruction of the community, are practically entirely
contained in the bodies of organisms, their concentration in the water
itself being close to analytic zero. The nutrient background of the surface
layer decreases as the water "ages," due to the constant loss of a portion
of the organic matter with the animals migrating into the depths and with
the descending dying phytoplankton and detritus. As the community matures,
it is carried with the water ever further from the location of the upwelling
and, therefore, the time picture of development of the community is unrolled
in space as well .

Since the upwelling of water occurs almost steadily, near the zone of
water ascent the community is constantly in the initial stages of its

14

development, with the maximum of phytoplankton,* while further downstream
in the current we observe the maximum of herbivorous zooplankton, which
requires more time for its development, and still further from the upwelling
zone we find the maximum of predators (Vinogradov et al . , 1961; Vinogradov,
Voronina, 1954; Vinogradov et al . , 1972; Timonin, 1971; Gueredrat, 1971).
Consequently, the maxima of the biomass of the various groups, which require
various lengths of time for their development, do not coincide in space
(Chapter II, Fig. 3).

The spreading of zones of predominance of various trophic groups
in space, accompanied by differences in number, biomass, dimensions and
vertical distribution of plankton, allows us to look upon the individual
stages in the development of the system as independent communities. Some-
times, this approach facilitates the study of the communities (Timonin,
1971; and others), since it allows us to ignore the degree of intermixing
of the various communities with each other. However, obviously, we should
always keep in mind that we are in fact analyzing and comparing not
steady-state pictures, but rather individual frames from a continuous
dynamic process.

The pelagic tropic communities require at least one or two months to
achieve the comparatively mature state characteristic of the ol igotrophic,
halistatic areas in the central waters of the ocean. During this time, the
community is carried by currents hundreds of miles from the region
where it was formed by the upwelling of the water.

Actually, in the tropical ocean, the water of various streams of
currents and the communities which it carries has significantly different
"age." Therefore, there is a constant, more or less intensive, mixing of
communities of varying degrees of maturity. Correspondingly, the
picture of development of a community which we have studied, and for which
quantitative mathematical models have been constructed (Vinogradov et al . ,
1972: Vinogradov et al . , 1973) is rather idealized. In actual fact, the
whole process is much more complex. First of all, the flow of water from
the upwelling zone does not form an integral whole. At various depths,
layers of water move at different speeds and in different directions.
Secondly, the picture which we have presented of the "primary" succession in
the ocean is rarely actually observed. It has been seen, for example, off
the coast of Peru, near southwest Africa and in certain other regions of
particularly intensive upwelling of water. Usually, however, the researcher

*If the rise occurs at 10"3-10"'^ cm/s or somewhat greater, i.e., if
the water rises by decimeters or meters per day, then a thermocline can form
directly at the point where the water rises, and a phytoplankton bloom is
observed. A bloom can develop in the rising water in three or four days
(Smith et al . , 1971: Strogonov, Vinogradov, 1975; and others). The more rapid
the rise of the water, the closer to the surface the thermocline forms;
if the rise is particularly rapid, for example, in the Peruvian upwelling,
the water may rise tens of meters per day (Smith et al . , 1971), the
phytoplankton cannot reach its maximum development at the point where
the water is rising, and the maximum is formed downstream from the point
of the water ascent.

15

encounters a situation in which the waters rise from depths which are not
very great, so that the waters which are rising are already populated by
a developed community. In this case, the entire system, even in the zone
of its formation, takes on a number of features which are characteristic
of comparatively mature communities (Vinogradov, Semenova, 1975: Flint,
1975). Finally, changes in wind speed also cause changes in the rate of
upwelling, while the axes of individual spots of upwelling of the water may
be significantly deflected, leading to mechanical scattering of concentra-
tions of zooplankton and phytoplankton at various depths (Stroqonov,
Vinogradov, 1975).

In SDite of the fact that, under actual conditions, there is constant
redistribution and mixing of communities, it is possible to observe com-
munities in the early stage of maturity, and use them to obtain some idea
of the basic regularities involved in succession changes. Obviously, in
order to clarify the cause-and-effect dependence of phenomena and processes,
we must study the entire picture of formation and development of the eco-
system. Isolated analysis of individual moments of its existence cannot
allow us to understand either the causes of the observed state of the
system, or its changes as time goes by.

2.3 The Succession of a Pelagic Ecosystem

The development of an ecosystem as time passes--its succession--is
one of the fundamental concepts of modern ecology. In the opinion of
Margalef (1958), succession in ecology occupies a position as important
as that of evolution in general biology.

Succession is a process of self-organization, which occurs in any
ecosystem. Margalef (1968) believes that any system consisting of repro-
ducing and interacting organisms and the environment must continue to
develop in the direction of creation of an organization for which the
value of entropy per unit of information stored and transmitted is minimal.
In the course of succession, structures (systems) are preserved which are
most able to influence the future at the cost of the least amount of energy.
In other words, the process of succession is equivalent to the process of
accumulation of information. As it occurs, the system changes in the
direction of achievement of a certain asymptotic steady state. In the
initial stages, the community receives its primary influx of information
from the surrounding (abiotic) environment, whereas in the more mature
stages, the significance of information transmitted from some components of
the community to others increases (Margalef, 1968).

This understanding of the succession changes in an ecosystem includes
changes occurring in developing communities in the pelagic zone of the
ocean. It is broader than the classical concept of succession, developed
by continental geobotanists , which has caused some authors to express doubt
as to the correctness of application of this term to the process of develop-
ment of aquatic systems.

However, the differences between continental and oceanic systems are
not differences of principle, but rather concern only certain of the
peculiarities of the phenomena and their quantitative expression.

16

The essence of these differences is that aquatic, particularly
pelagic, systems have a much greater degree of "openness," than do
terrestrial systems. The great changes in the biotope in these systems
occur primarily under the influence of abiotic factors, and they depend
more than terrestrial systems on the arrival of nutrients from without.
Furthermore, the concept of the final state (climax) in pelagic systems is
less definite than in continental systems; however, this problem is less
disturbing if we speak not of the climactic state of the system, but rather
of its greater or lesser maturity.

It should be noted that the exploitation* of aquatic, particularly
pelagic, systems, as a rule, is significantly higher than that of terres-
trial systems. The extraction of organisms from the primary layer of
habitation to depths unsuitable for their existence, the loss of organisms
carried away by currents beyond the optimal area of habitation, the
inroads of predators, all occur in pelagic systems with great intensity
and encompass the overwhelming majority of the plankton population. The
stronger exploitation, as is the case in terrestrial systems, retards or
prevents the achievement of maturity by the system. From this point of
view it is interesting that plankton systems reach relative maturity
only in stratified water with weak intermixing, where the loss of phyto-
plankton cells from the euphotic zone is minimized.

One defining aspect of succession in the pelagic zone is the
accumulation by the community of energy in the initial stages of its
development and the preservation or expenditure of this store of energy
in its more mature stages. Naturally, energy losses also occur in the
early stages, energy accumulation in the more mature communities, but in
the initial stages the processes of assimilation of energy, on the
average, prevail over the processes of dissimilation, while, with the
development of the community, this picture usually changes.

We emphasize once more that as pelagic zone ecosystems age and
mature, changes occur not only in the biotic component--the community,
but also in the biotope itself. First of all, the stratification of the
layers of water becomes more stable, facilitating differentiation of the
population and increasing the stability of the entire system.

What are the structural and functional changes which occur in a
pelagic community as it matures? A summary of all available information
on the succession of pelagic communities would occupy far too much space
and is therefore not expedient, particularly if we consider that attempts
have already been made in this direction (Margalef, 1958, 1962; Vinogradov
et al., 1973; Gueredrat et al . , 1972). Nevertheless, the primary trends
in the changes should be analyzed.

*"Exploitation" of a system refers to any removal of living organisms
from the system (Margalef, 1968).

17

2.4 Changes in Structural Characteristics

The accumulation of information as the system matures leads, first
of all, to an increase in the variety* in the community. However, it should
be kept in mind that in mature communities, organisms which are taxonomically
or trophically similar tend to form local accumulations, which decreases the
variety encountered in small volumes of water. Nevertheless, the signifi-
cance of variety for any individual is rather constant in various systems
and increases as their maturity increases. Thus, for marine phytoplankton
it varies from 1.4-2.0 bits (per individual) for young systems to 3.5-
5.5 bits in later stages of succession (Zernova, 1974; Blasco, 1971).
The upper limit of variety is not over 4.5-5.5 bits, which, possibly, is
the limit of effectiveness in the construction of natural self-regulating
systems.

The increase in variety which results from any ecologic succession
or any process of self-organization of ecosystems touches the most varied
characteristics of the community. For example, Margalef (1968, etc.) con-
siders an increase in the variety of pigments to be a characteristic sign of
the development of a phytoplankton community. However, the increase in
variety is manifested most clearly as a change in the species composition of
the community as it matures.

An increase in variety has been clearly demonstrated in the community
of the tropical regions of the Indian Ocean (Timonin, 1971). In the
regions of upwelling water--in the early stages of development of communities--
the index of species variety of zooplankton was found to be 1.5-2 bits,
while as the communities developed it increased to 2-2.5, and in comparatively
mature communities in stable, stratified water, it reached 3.5-4 bits.

Simultaneously with species variety, trophic variety also increases
(Fig. 2). In the early stages of succession, we find primarily nonspecial ized
herbivores or omnivores, while in the later stages, species with more
selective feeding, consuming larger food items, predominate. The increase
in the share of macrophages (predators) and the lengthening of the food
chains are characteristic for mature oceanic systems (see Chapter II,
paragraph 1 ) .

The changes in the store of energy in a community are primarily
manifested as changes in its biomass. In the initial stages of development,
be it in spring in cold-water zones or in a region of quasistationary
upwelling of water in the tropics, the biomass increases rapidly and is
initially concentrated in the most labile link of the chain--the phyto-
plankton. At this time in the euphotic layer there is a store of nutrient
substances, usually intensively replenished by the upwelling of the deeper
water. In later stages, most of the nutrients of the system are concentrated

*When speaking of variety, we should keep its spectrum in mind, since
in individual small samples the variety of various systems may be identical,
in spite of great differences in variety of the general sets involved.

18

'^,0
J,S
3,0
2,S
2.0

Htr/bit(g)

# r^v^y V.::\ff

"^

Fig. 2. Structural changes in the zooplankton communities with changes in
the nature of vertical movement of the water (Timonin, 1971). I, Zone
of intensive divergence; II, Intermediate zone, weak upwelling of water;
III, Zone of convergence or stable stratification of water; B, Total biomass
of zooplankton; Hsp, Species diversity; Htr> Diversity in trophic structure;
1, Swallowing predators; 2, Biting predators; 3, Sucking predators;

4, Animals with mixed feeding (omnivores); 5, Coarse filter feeders;

5, Fine filter feeders.

in the bodies of its organisms. Soon, processes of dissi
to predominate in the community and the total mass of pi a
The maximum biomass, as the community develops, tends to
trophic chain--first to the herbivores, then to the preda
leading to basic changes in the trophic structure of the
picture of displacement of the maximum of biomass upward
chain is clearly demonstrated by a model of the functioni
community (Vinogradov et al., 1971, 1973) (see Fig. 5.4)
observations (Vinogradov, Voronina, 1964; Tinomin, 1971;

milation begin
nkton decreases,
shift along the
ceous forms,
community. The
along the trophic
ng of a tropical
and by field
Gueredrat, 1971).

The increase in the mean dimensions of organisms as a community
matures touches both phytoplankton and zooplankton. As the community
matures, the significance of larger animals (macroplankton and micronekton)
increases, while the mean dimensions of the animals of the mesoplankton and
microplankton increase. For example, in the South Atlantic as we move from
the South African upwelling to the central halistatic regions, the mean
weight of microplanktonic and mesoplanktonic organisms increases by a
factor of 3-3.5, while the fraction of mesozooplankton in nets and water
bottle plankton from the upper 200 meter layer increases from 2/3 to 4/5 of
the total mass of animals (Kovalev et al . , 1976). As the biomass decreases
and the mean dimensions of organisms increase, as we have seen, the variety
of the community increases (see Fig. 2), i.e., these processes act as if
they were inversely dependent (Sutcliffe, 1960; Longhurst, 1967; Timonin,
1971; etc.).

19

2.5 Changes 1n Functional Characteristics

The succession changes in biomass and trophic structure of communities
are closely related to changes in their functional characteristics. The
difficulties of quantitative evaluation of most of these usually force us
to give only a qualitative estimate of many functional characteristics.
However, the efforts expended in recent years in the study of pelagic eco-
systems have in many cases allowed quantitative characterization of the
succession changes in production not only for the lower trophic and ecologic
groups (phytoplankton, bacteria), but also for higher levels and for the
entire community as a whole, as well as estimation of the changes which
occur in the course of succession in a number of other functional parameters;
the degree of satisfaction of the demand for food (6), the stress on trophic
connections [e, or k), the degree of balance of production and consumption
of various trophic levels (e) and their ecologic effectiveness (w).*

*According to Slobdkin (1961), Menshutkin (1971), Vinogradov et al .
(1976), 6 = Ri/R*^^^, where R^ is the actual ration, i.e., the food which an
animal can consume given the available prey, R^^^ is the maximum ration,
i.e., the quantity of food which the animal could consume to support its
maximum growth rate.

" max

r' III
I'^i

1

J -Pj

" max

where ^^r^^ is the sum of the particular maximum rations of consumers,

i
Pj is the production and Bj is the biomass of prey;

n

max

v.. = is the index defining the pressure of

predators on the biomass of a given prey species. These last two parameters
show the extent to which, under the conditions present, organisms of the j^^
group can be consumed and the extent to which the food requirements of
consumers can be satisfied by the production of the prey;

^j

Pj
-^ — is the ratio of prey production to the sum total

i^u

of the particular rations of predators, and shows the extent to which the
production of a lower trophic level is utilized by organisms of the sub-
sequent trophic levels;

20

As M. E. Vinogradov, E. A. Shushkina and I. V. Kukina (1976) have shown,
in the early stages of development of a community with high biomass of
autotrophs, the nutritional demands of the animals of all trophic levels
are satisfied to a high extent (6 - 0.8), supporting an increase which is
close to the maximum. As the community matures, the degree of satisfaction
of the nutritional demands decreases (6 ~ 0.4-0.5). As 6 decreases, the
stress on the trophic connections between organisms at various trophic
levels increases. The trophoecologic coefficient k, showing the measure of
pressure of consumers on the biomass of a given species, is less than 1 in
the early stages of development of a community for practically all of its
elements, whereas in more mature stages, particularly for the lower trophic
levels, it increases rapidly.

On the basis of qualitative assumptions, it would seem probable that
as a community matures, the degree of balance between production and
consumption would increase. However, calculations show that the change in
the degree of balance occurs quite differently at different trophic levels,
and the assumption is valid only for some of them. Actually, the production
of phytoplankton or bacteria may be underutilized, not only in the early
stages of succession of the community but also, under certain conditions, in
later stages, meaning that the general discussion of the degree of balance
of production and consumption in communities of various stages of maturity
and various trophic structure is not well founded.

The ecologic effectiveness of transmission of energy from one trophic
level to another (w) increases with increasing trophic level, and also
as the community matures and the degree of satisfaction of nutritional
demand decreases.

Calculations of change of the actual (P) and specific (P/B) production
of various trophic levels of a community as it matures, performed for
communities around the eastern Pacific equatorial upwelling (Sorokin et al . ,
1975a; b; Vinogradov et al . , 1976) have shown that the production of the
lower trophic levels (phytoplankton, bacteria, protozoa) decreases with
maturation of the community more strongly than the production of mesoplankton,
particularly predaceous forms. In certain groups (protozoa, predaceous
mesoplankton) in a mature community the actual production may be negative,
a result both of their increased consumption by other animals and of
cannibalism within the group itself.

I nj

^ij

— is the index of the deqree of utilization of the

energy accumulated in a lower trophic level by the next higher trophic level.

21

The specific production of various elements of the community may also
vary significantly as a function of the trophic relationships which develop
in the community in various stages of its development. In general, as
the community matures, the specific production of certain of its elements
decreases, and in certain cases becomes negative (Vinogradov et al . , 1976)
(Fig. 3).

Fig. 3. Change in daily specific pro-
duction (P/B) of various elements of a
plankton community as upwelling weakens
at the equator in the eastern Pacific
(Vinogradov et al . , 1976). 1, Phyto-
plankton; 2, Bacteria; 3, Protozoa;

4, Herbivores and Omnivores;

5, Carnivores; I, 97°W; II, 122°W;
III, 140°W, IV, 153°W.

The actual and specific production of a zoocenosis and of an entire

community are comparatively high in the early stages of development of

the community, then decrease sharply or even become negative in the more

mature stages, as dissipation of energy begins to occur in the community
(Table 1).

All of the above leads us to the realization of the magnitude of the
structural and functional changes experienced by a pelagic community as
it grows and moves together with the water. Obviously, as we compare the
ecosystems of various localities within a single large region, we should
always keep in mind possible age differences of the communities, which may
be responsible for many of the differences observed. Only a dynamic,
succession approach to the study of ecosystems allows us to understand the
causal dependence of the processes occurring within them.

22

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23

3. Nontrophic Regulatory Interactions of Marine Invertebrates.
(E. A. Zel ickman)

3.1 Metabolic Regulation

Chemical communication is the most ancient of all systems of exchange
of information between organisms and, correspondingly, of regulation of
intrapolation and intraspeci fie relationships. The chemical substances
excreted by plants and animals into the water are elements which communi-
cate and regulate the activity of the community, modifying the numbers of
individuals of the species. They may be attractants, repellents, may
facilitate the development of certain species and suppress others, etc.
These allelopathic relationships are well known in continental phytocenoses ,
vertebrates and insects as well. The species-specificity of metabolic
signals in certain cases has been experimentally proven. Lukas (1954)
referred to this type of relationship as nonpredatory ecologic connection.
These connections are achieved by chemical agents with a broad spectrum of
action which, after they are liberated into the water, become an environ-
mental factor for the organisms in the community. Exocrines may be products
of excretion or of decomposition of organisms.

Some marine bacteria excrete metabolites which are toxic for algae, thus
changing the population of the latter (Berland et al . , 1972), In water rich
in diatoms, the population of blue-green algae will not be great (Marumo,
Asaoka, 1974). The excreted metabolites can be considered for neighboring
organisms a method of adaptation to the interrelationships in the community.
This type of metabolic interaction relates the population of the diatom
Skeletonema costatum and the flagellate 01 isthodiscus luteus (Pratt, 1966).
In a medium favorable for both species, they cannot achieve simultaneous
abundance. The advantage will go to that species, the cells of which begin
intensive division with larger numbers or at a younger phase of the
population. The substance excreted by the flagellates simulates cell
division of the Skeletonema in a rarefied culture of diatoms, and depresses
cell division in a compact culture. In a community, these species have
different survival strategies, which can be interpreted as behavior in
the broadest sense: The diatom must "try" to begin its first division
with a large number of cells; the flagellate conducts "chemical warfare"
with it. The Skeletonema may suppress (or stimulate) the growth of
bacterial cells as well (Be et al . , 1974).

Suppression of a competing species by means of "chemical weapons" is
a common occurrence in the sea. When the hydroids Hydractinia echinata
and Podocoryne carnea are simultaneously cultivated, their stolons never
interweave, and after a certain period of time, Podocoryne completely
suppresses the growth of Hydractinia (Gallien, Govaere, 1974). The same
type of interaction, but intraspecific, may regulate the number of individ-
uals in clusters of the hydromedusa Tiaropsis multicirrata (Zelickman, 1969;
Zel ickman et al., 1969).

24

Succession itself may be, to a significant extent, a result of
dynamic integration (inhibition of neighbors or self-inhibition) of the
community, mediated by exocrines. This aspect of the significance of
free metabolites facilitates the development of new connections between
species and the occupation of new habitats. The exocrines indirectly
regulate the populations, marking out the path of migrants, facilitating
encounters between the sexes, unmasking prey, marking spots for settling
of larvae, etc. This indicator role of external metabolites is no less
significant than the "plus-minus interaction" reactions mentioned above.

3.2 Pheromone Regulation

The steroid compounds, the derivatives of which usually serve as
moulting and juvenile hormones, as well as sexual pheromones, are inherent
in all types of invertebrates. Pheromone regulation, in particular, is one
type of exocrine regulation. When in the process of evolution specialized
receptors developed on the one hand and, on the other hand, the hormones
of the donor began to be liberated into the environment, communication by
means of pheromones became possible (Kittredge, Takahashi, 1972). The
sexual pheromones have been most thoroughly studied to date. It is
possible that they appeared earliest in the course of evolution. Usually,
a sexual pheromone is a relatively species-nonspecific substance liberated
into the water, causing swarming of individuals of both sexes and subsequent
emission of reproductive products, e.g., in the polychete Platynereis
dumeril ii (Boilly-Marer , 1959). In the polychete Ophryotrocha puerilis,
sexually mature females liberate into the water a substance which stimulates
the development of male sexual characteristics in immature individuals.
The females of many nereids excrete species-specific substances which
accelerate the discarding of sperm by the males. The males of the polychete
Grubea clavata produce a substance which facilitates emission of eggs;
without this substance, the eggs are resorbed in the bodies of the females.
The ability to attract males or females, preferably of only the same species,
is evolutionarily more progressive; this occurs, for example, in the
gastropod Littorina littorea (Dinter, 1974).

The species specificity of sexual pheromones is relative and does
not assure complete reproductive isolation. For example, males of the
copepod Eurytemora aff inis demonstrate searching sexual behavior and
"chase" not only females of their own species, but also females of E.
herdmani and Pseudodiaptomus coronatus. However, the males of the latter
two species demonstrate sexual behavior only toward females of their own
species (Katona, 1973). The searching behavior of Calanus and Pseudocalanus
is equally expedient (Griffiths, Frost, 1976).

Even in the decapods, the larval hormones and sexual pheromones have
still not completely biochemically diverged. The crustecdyson of the
decapods usually acts as a pheromone in combination with any other pheromone,
causing onset of the stage of maturation of the female. The females of
Homarus americanus, just after ecdysis, liberate a pheromone which suppresses
the aggressiveness of the males and provokes sexual behavior in them.
However, if females are forced to moult by removal of the eye stalks, the

25

water from an aquarium containing these females causes only mild manifesta-
tion of searching sexual activity. When males contact females which have
not moulted, only aggressive behavior is manifested (Atema, Engstrom, 1971).
The males of many crabs , e.g. , Carcinus maenas , Macropipus hoi satus and
others (Bales, 1974), assume the mating position only in the presence of
females which have recently moulted or are in the premoulting stage.
The pheromone is species-specific and is excreted with the urine.

Thus, the contact of the sexes at the biologically most favorable time,
and reproductive isolation are assured in many cases by the chemical
communication channel. The functions of this channel, the end result of
which is aggregation of the animals, have many aspects, like all manifesta-
tions of topic connection. One means of aggregation is excretion by mature
animals of substances which stimulate settling of meroplanktonic larvae.
The larvae of barnacles, in which this phenomenon was demonstrated for
the first time (Crisp, Meadows, 1963), respond only to the "settlement
factor" if it is found on a surface suitable for settlement in all its
parameters .

The bentbic predators freauently excrete substances which "mark" the
place where prey is found. Thus, hungry Acanthaster planci sea stars move
more rapidly toward coral (their only food) on which A. planci are already
feeding (Ormond et al . , 1973).

Chemotactic communication as a means of recognizing individuals of
one's own species (not necessarily of the opposite sex) results in the
formation of aggregations and also acts as a mechanism for regulation of
numbers. This is well known in the planaria. Phagocata gracilis and
Cura foremani , mixed together in a single vessel to the point of random
distribution, regroup in single-species clusters quite rapidly. The
adaptive value of this form of behavior consists in that P_. gracil is lays
its egg capsules only in clusters of at least 200 individuals (Reynierse,
1957; Reynierse et al . , 1969). Dugesia tigrina spontaneously decapitates
when greatly crowded--one individual per 10 ml of culture fluid. It is
assumed that the metabolite causing this phenomenon suppresses asexual
reproduction of the planaria, replacing the neurohumoral stimulus for
reproduction (Vowinckel et al . , 1970).

Frequently, the level of activity of an animal and its diurnal
rhythm depend on the number of individuals in the group, increasing with
increasing number of individuals up to a certain limit, then sometimes
decreasing. The manifestations of the group effect are various, although
the mechanism of the phenomenon itself is frequently unclear. For example,
in males of the gastropod mollusks Crepidula fornicata, joining of the
mollusks into chains of several individuals activates the growth of all
the individuals except for the uppermost male, the growth rate of which
is the same as that of an isolated male (Le Gall, 1973). In a mixed culture
of three species of Black Sea mollusks, the oxygen consumption and growth
rate were both lower than for single-species cultivation under the same
conditions (Kiseleva, 1974). In any case, the metabolites have a direct
relationship to the regulation of growth of the members of a community.

26

Maintenance of nongregarious burrowing animals, Homarus americanus,
in a group for some time subsequently decreased the aggressiveness of
these individuals when they were placed individually into aquariums with
one Homarus and one place of refuge (Dunham, 1972). "Swarming pheromones"
similar to those of many insects have been found in crustaceans: They are
present in Saron marmoratus and many hermit crabs (Hazlett, 1966). Thus,
the group effect and mass effect are manifestations of the initial phases
of formation of nontrophic group communication.

Chemical protective substances, temporarily blocking the mobility
of an enemy, are known in plankters. For example, the medusa Aequorea
aequorea excretes a substance which inhibits the movement of the medusa
Stomotoca atra (Lenhoff, 1964), which frequently eat coelenterates. One
variety of protective pheromone is the alarm substance, which is also quite
widespread among aquatic invertebrates. If viscera of the sea urchin
Diadema antillarum contact the water, a substance is liberated which
causes other sea urchins to flee the area of danger.

One special type of intraspecies signaling, intended to aid in
nocturnal visual reception, is bioluminescence. In females of the euphausiid
Meganyctiphanes norveqica, the periods of maximum response to the luminescent
flashes of the males correspond with the periods of attachment of the
spermatophores; thus, luminescence can be looked upon in this case as an
attribute of sexual behavior (preparedness signal). Imitative (response)
luminescence has been detected in the same animals (Kay, 1965; Tett, 1972).
In the ctenophorans Beroe and Bol inopsis and the hydromedusa Aeginopsis
laurentiae, a flash can cause a defensive motor reaction (Labas, 1973).

3.3 Interspecific Collective (Group) Reactions

Group reactions which tend to support coexistence of species due to
negative contacts can be considered aggressive relationships. These
relationships are possible when the ability to recognize objects in the
surrounding world is developed. The most primitive form of collective
behavior is direct destruction of the neighboring species not for the
purpose of eating it. Recognition of the object in this case apparently is
chemoreceptor mediated. By this method, the madrepore corals, secondary
in terms of abundance, which construct relatively small and slowly growing
corallites, protect themselves from the dominant, more rapidly growing
forms: the more aggressive, slowly growing species destroys the polyps of
the other species, dissolving their tissues with mesenterial threads (Lang,
1973). This is a simple case of group behavior with a direct topic (to use
the terminology of V. N. Beklemishev, 1951) connection. However, the coral
reef biotope is also the site of indirect connections. A complex form of
group interspecies behavior with indirect topic and phoric connections is
seen in the relationship between fish and sea anemones and between hermit
crabs and sea anemones. The symbiotic relationship between the fish
Pomacentridae and the sea anemones of the family Stoichactidae is well known
iDhont, 1971; Mariscal , 1970). Frequently, one corallite, one sea anemone,
the mantle cavity of one tridacna or one sponge osculum is occupied by a
single pair of fish, shrimp or crabs, monopolizing the tiny microbiotope.

27

Sometimes one corallite is inhabited by a single pair of crabs of one
species, which is achieved by intraspecies agonistic behavior (Preston,
1973). Twelve species of fish of the genus Amphiprion are obligate
symbionts, exhibiting territorial behavior (protection of "their" sea
anemone as long as they are located near it). If the anemone is removed, the
territorial behavior decreases, and the feeding and aggressive forms of
behavior are altered. The closeness of direct and indirect topic and
phoric interdependence can be quite varied; for example, in the various
species of Amphiprion or among shrimp from the families Hyppolytidae,
Alpheidae and Palaemonidae, associated with a broad range of benthic
invertebrates and even pelagic scyphomedusan (Bruce, 1972; Fankboner, 197?).

In representatives of the mobile epifauna, the primitive form of
collective reactions is rather passive. Thus, the brittle stars Astroboa
nuda form unusually close settlements in the shallow waters of coral reefs.
The arms of the individuals intertwine, forming a dense net across the
direction of the current. This "plankton net" assures effective, nonselec-
tive filtration of the bottom-dwelling copepod (Tsurnamal , Harder, 1966).
It has been shown that each star occupies the same position each night, and
retreats to the same shelter each day (Fricke, 1973). Similar behavior is
exhibited by Ophiothrix gracil is.

Any systematic encounter of individuals, resulting in a change in the
course of individual motor reactions or combinations of motor reactions,
must be considered an evolutionarily more advanced form of group ("social")
behavior. Strictly speaking, nongroup, purely individual, behavior, in the
precise sense of this word, cannot be achieved in nature, since some
minimal interaction between individuals always occurs, at least in some
stage of ontogenesis. However, obligatory group behavior is the most fully
integrated form of living activity, though its population adaptiveness is
not always obvious. This category of nontrophic connections must include
all aspects of intra- and interspecific domination-subordination relation-
ships (Wynne-Edwards, 1962), since they also regulate the size of populations
and increase qualitative variety of genotypes due to complete or partial
elimination of a number of "unsuitable" individuals from the breeding pool.
Thus, after establishment of a hierarchy in a group of Diogenes pugilator
hermit crabs, the dominant male eats more food and moults more frequently
than the subordinate males (Rossi, 1971). In the Dardanus arrosor hermit crabs,
living in symbiosis with the Calliactis parasitica sea anemone, the anemone
is always captured by the dominant crab, regardless of whether it already
has a symbiont on its shell or not. The subordinate crab does not take
an anemone in the presence of the dominant crab, even if the shell of the
dominant crab is already occupied by anemones, so that a free anemone has
fallen to the bottom (Mainardi, Rossi, 1969). In the squid Lol igo
pealei , a hierarchical structure of behavior of the males during breeding is
observed. When there are more males than females, the subordinate males
are not allowed to mate. The hierarchical behavior is not manifested
during feeding (Arnold, 1962).

Competition between an individual and a group is frequently replaced
by ritualized behavioral elements, a sort of "psychic attack" (Severtsov,

28

1951, p. 94). Ritualization is useful to the species, since it retains
the most reproductively valuable males. There is another means for
elimination of the contradiction: inter- and intra-species aggressiveness
helps to scatter individuals over the maximum number of microbiotopes within
the limits of their area of distribution. Ritualization is highly differ-
entiated in decapods and, in a number of ways, is comparable to that of
birds (Hazlett, 1972b). The hierarchy within a population arises in the
process of aggressive collisions between animals, but after it is established,
battles, as in the vertebrates, are replaced by ritualized behavior. The
previous group contacts among decapods are important for the results of
encounters between males: If in a previous battle a male won, it is probable
that he will win again in a later battle with an opponent of equal size.
Superior size, initiative in beginning the conflict and the experience of
previous victories increase the chances of success in encounters (Mainardi,
Rossi, 197?; Rubenstein, Hazlett, 1974). The position of the legs and claws
during agonistic reactions in the crabs Microphrys bicornutus are more
strictly fixed than during walking and feeding, allowing the crab to recognize
the intentions of the enemy, by comparing its behavior with the stereotype
(Hazlett, 1972a). The strategy of the victor in a battle between hermit
crabs consists in the best possible adaptation of his own behavior to the
behavior of the enemy, while the behavior of the loser always contains
greater elements of chance (Hazlett, Estabrook, 1974).

However, true battles arise (for example, among Callinectes sapidus)
only when ritualized attempts to stop a crab approaching food or a female
are unsuccessful (Jachowski, 1974). Ritualized aggressive behavior for
the protection of individual territory is clearly expressed even in
certain individual species with no hierarchy, such as Muni da sarsi
(Berrill, 1970). The degree of correlation between ritualized behavior
and the defense of the territory, may change as a function of local
conditions. For example, Dardanus arrosor, after losing its sea anemone,
is more frequently attacked by other members of the same species. When
there is a shortage of food or an increase in the number of crabs, they
more frequently place an anemone on their shell. After many months in
an aquarium, hermit crabs lost their anemone-seeking activity, but when
an octopus was placed in the aquarium, this behavior was reactivated
(Balasch, Mengual , 1974). Aggressiveness is differentiated with respect
to mature and young animals, a behavioral adaptation to protection from
cannibalism. For example, in the hermit crab Clibanarius vittatus, if
there are great differences in the sizes of two individuals, the larger
crab often simply ignores the smaller one (Hazlett, 1968).

Relationships in a group are not always aggressive in nature. The
decrease in aggressiveness observed following long-term cohabitation of
Pagurus bernhardus, with an outbreak of aggressive behavior toward a new
individual, are apparently explained by the capacity for individual rec-
ognition (Hazlett, 1969). The shrimps Hymenocera pi eta live in pairs,
generally of different sexes. A male and female usually sit side by side,
side, undertaking no sexual activity and not feeding. The partners have a
quieting effect on each other. Isolated males seek out only their own
partner (Seibt, Wackier, 1972). The shrimp Stenopus hispidus fight to the

29

death when they meet an individual of the same sex, but when a male and
female meet, the female assumes the subordinate position, and a long-
lasting pair is formed (V. R. Johnson, 1969). In this behavior we can see
the primordial form of monogamy inherent in vertebrates, indicating the
convergent evolution of behavioral mechanisms in various branches of the
animal kingdom (Wickler, Seibt, 1972). Analysis of behavior as one aspect
of ecologic adaptation (Reese, 1964; Fricke, 1973) shows that convergent
evolution is unavoidable. Thus, aggressive behavior in species which are
territorial should be suppressed for successful mating, which is achieved
by the use of the subordinate pose by one of the partners, though the
specific manifestations of this ritual in various taxonomic groups are
different. General systems of behavior, characteristic for certain life
forms, change, adapting to the specific demands of each species. Therefore,
in highly specialized commensals, programming of behavior varies most
widely from the general system. The specific manifestations of the general
features of behavior depend greatly on the development of receptors. For
example, in lower crustaceans and gastropods, ritualization (if it is
present) depends to a greater extent on the perception of the chemical and
vibrotactile stimuli than visual stimuli. Naturally, behavioral adaptations
are particularly complex in wery complex biotopes with sympatric speciation.

The trigger mechanisms of group reactions may depend on any receptor
system. The key stimulus may be either an abiotic signal or information
from another organism. The capability for group reactions may be initiated
by the diurnal rhythm of abiotic factors. For example, the distribution of
male Ilea pugilator crabs is group-determined before the tide flows, while
during the flow of the tide it is random; during tidal flow, the females
form groups (Rajendran, 1974). Individual burrowing decapods Goneplax
rhomboides and Nephrops norvegicus are usually active during the dark hours,
but the presence of other individuals of the same species inhibits this
activity (Atkinson, 1974). The presence of other individuals is also
significant in other respects; disruption of territoriality, e.g., in
lobsters, results in atypical migration, making them prey to predators
(Chittleborough, 1974).

Orientation among other similar animals is a result of complex
functioning of receptors; territorial behavior, as a variety of group
behavior, does not always include continuous communication with another
individual of the same species. Arbitrary interruptions in communication
are permissible with wave translation. The reception of information by
means of vibrotactile receptors is widespread. It is in this manner that
sagittae detect Copepoda: The hunting sagitta hangs motionless in the
water until it senses vibrations at a specific frequency. Possibly, each
species of chaetognaths has its own specific range of perceived frequencies
(Newbury, 1972). In the land crab Gecarcinus lateralis, intraspecies
communication is achieved by the vibration of the substrate by each indi-
vidual with a definite sequence of pulses (Klaassen, 1973). The Ocypode
crabs also react to vibrations of the substrate, emitting response signals
at the corresponding frequency (Horch, Salmon, 1972). The threshold
frequency for beating of the barnacles is species-specific; therefore,
representatives of different species respond differently to the identical

30

stimulus, allowing them to coexist (Blaker et al . , 1964). It has been
experimentally shown that in Balanus improvisus, information on the condition
of a neighbor influences the mechanoreceptors, the micropopulation "tuning"
itself to the rhythm of beating of the most active individual (Vilenkin,
Vilenkina, 1971; Vilenkin, Zaikin, 1975).

3.4 Intraspecific Structures of Behavior of a Group of Individuals

One means of avoiding competition where ecologic niches overlap is
heterogeneity of the spatial distribution of micropopulations, hemipopula-
tions or groups of other ranks with different types of behavior. Hetero-
geneity, in particular, may result from a group response to gradients in
biotic or abiotic environmental conditions. These responses are most
typical for nonpredatory animals. The most important methods of formation
of discreteness probably differ in organisms of different sizes, but they
all lead to an increase in the isolation of groups.

Schooling may disappear or appear under certain conditions. For
example, the cladoceran Polyphemus pedi cuius, in an aquarium with sufficient
food, normally live and breed individually, but in plankton live only in
groups with "jery constant locations (Butorina, 1972). Butorina considers
the group to be a food-hunting association of voracious predators feeding
on prey which also live in groups. The group of predators includes
individuals with identical spectra of prey, similar nutritional demands
and compatible speed of movement. When the population density is low, these
groups do not form (Luferov, 1970; Luferov, Stetsenko, 1971). Moina swim
in fish-free areas in dense schools, simultaneously changing direction and
retaining their order. However, in the presence of predatory fish, schools
do not develop (D. S. Johnson, Chua, 1973).

Underwater observations have established the existence of schooling
in the Copepoda Arcatia spinata, Oithona nana, 0. oculata, Farranula
gracilis and others (Emery, 1968). A school of Farranula gracilis acts like
a single individual and holds its position against the current. If alarmed,
the animals scatter, but then the school reforms. The density of Copepoda
in the school may be as high as 105 indiv./m3.

The reasons and mechanisms of formations of clusters, aggregations and
schools differ for different forms of life, and also for large and small
organisms. For nonselective filter-feeders--Appendicularia--which seem to
be poor swimmers, the "collective force" may create local hydrodynamic
factors, simultaneously facilitating increases in phytoplankton concentration.
Clusters of Oikopleura dioica (concentration on the order of 10^ indiv./m^)
have been described several meters wide and several kilometers long,
developing in the region of a phytoplankton bloom (Seki, 1973). Clusters
of Oikopleura frequently form parallel strips up to 30 m long, with a
width and depth of a few centimeters. Owen (1967) considers small-scale
horizontal surface vortices which develop at lines of convergence, i.e.,
Langmuir circulation, to be responsible for these clusters. It is possible
that the movement of these strips of Oikopleura helps to reduce the
resistance of the water, due to the mucus which the animals excrete.

31

The overwhelming majority of species of Copepoda and Ostracoda show a
tendency to aggregation (Fasham et al . , 1974). Aggregations* may be
differentiated depending on sex, age and physiologic condition of individuals.
In the copepod Epilabidocera amphitrites, accumulations of the crustaceans
near the surface of the water consist only of males, which differ from the
females in that they exhibit phototaxis (Park, 1965). In Metridia longa, the
microdistribution of the older copepodites differs from the distribution of
sexually mature individuals, which inhabit the same layer of water
(Romanovskiy, Chusova, 1974). Doubtless, this sort of heterogeneity is
adaptive. An example is the Monstril loida , semiparasites of sublittoral
invertebrates. Their hosts live in clusters, and it is not surprising
that the crustaceans themselves are also clusterers. The grouping of
hosts helps the nauplii to find hosts, while the grouping of the
monstrilloidae themselves facilitates simultaneous emission of nauplii
and their settlement (Isaac, 1974). This increases the level of inbreeding
in the population, which in turn facilitates sympatric speciation, i.e.,
the development of heterogeneity at a higher level.

Among the Decapoda, schooling is widespread, the characteristics
of the school being frequently quite homogeneous. Schooling is most common
among surface-dwelling species, for example, the shrimp Sergestes similis,
which forms accumulations with densities of up to 4500 indiv./m^ (Omori et
al., 1972).

Mixed aggregations are also found, consisting of individuals of various
species, e.g., the shrimp Acetes kochinensis and various genera of
amphipods (Achuthankutty et al . , 1973). The" reasons for formation of this
type of aggregation are not clear. In the pelagic crabs Polybius henslowi
and Charybdis edwardsi , surface schools contain individuals of both sexes,
oriented against the current and precisely observing their distance (J. A.
Allen, 1968; Delia Croce, 1961; Delia Croce, Holthuis, 1964, 1965; Rice, 1969).
Another method of observation of distance is the movement of crustaceans in
chains during seasonal migrations of the Stomatopoda Oratosquil la investigatoris
(Losse, Merrett, 1971) and the lobster Panulirus argus (Herrnkind et al . ,
1973). The lobsters move one after another, with their antennae or
pereopods touching the abdomen or tail of the lobster in front; a single
column may include as many as 65 individuals. During brief stops, the
lobsters also stay in an organized cluster, e.g., a "rosette."

3.5 Adaptive Value of Schooling Reactions

The collective reactions of plankters, during which the school reorganizes
or is restored, consist of a combination of behavioral events which take
consideration of the behavior of neighbors.

*The word "schooling," in our terminology is used to stress the active
role of inner factors in forming an aggregation and the intensity of
interdependence between the individuals.

32

Schooling is related to the manifestation of stereotypic reactions
based on signal simplicity, speed and accuracy of action. Manifestations
of schooling behavior in pelagic animals of various taxons have a great
deal in common. The information which supports the schooling behavior
can pass through many channels. The motivation may also be varied.
Defensive motivation is most common: Schooling, an essentially little
structured system of behavior, is a useful defensive response when
pelagic animals are under attack by predators. The sequence of motor
events is adaptive and constant for the group, but the trigger (liberating)
stimulus for these behavioral programs can vary. It is assumed that the
formation of groups of any repetitive type is a manifestation of protective
reactions. Attempts to analyze schooling experimentally (Radakov, 1972;
Neill, Cullen, 1974 and others) have shown that schools definitely play
a protective role among prey animals. Among predacious fish, squids
(Loligo vulgaris) and cuttlefish (Sepia officinalis) , the absolute and
relative number of successful attacks on the prey decrease as the number
of fish in the field of vision of the predator increases. An increase
in the number of fish (prey) in a school retards the beginning of the
attack and makes the capture of prey by attackers more difficult.
Schooling of the prey dissipates the attention of the predator, confusing
the stereotype sequence of the individual stages of the chase, and the
attack is frequently not completed. The usefulness of the school when
the predators are herding types has been proven for squid (review:
Nesis, 1975) and fish (Radakov, 1972).

Let us discuss the phenomenon of schooling in euphausiids and mysids,
in which it is frequently seen and has been relatively well studied, in
somewhat more detail.

Among the euphausiids, phytophages predominate: Thysanoessa longipes,
J. inermis, J. raschii , Meganyctiphanes norvegica, Euphausia superba, E.
crystallorophias, E. vallentini (Zelickman, 1961b, 1968b; Marr, 1962), forming
schools and clusters near the surface. A euphausiid school is a practically
single-species organized group of animals, recognizing each other (main-
taining distance}, of relatively homogeneous physiologic structure. Among
Barents Sea euphausiids, as exceptions, we observed three-species schools,
but always one species dominated. In most cases, the term "school" is
applied only to mature individuals. A school may be scattered by external
actions, after which it immediately reforms. The dimensions of a school
vary from a few meters (Nemoto et al . , 1969) to 30-100 m and greater
(Pavlov, 1974; Marr, 1962; Nemoto et al . , 1969). The shape of schools of
Euphausia pacifica, E_. similis, E. nana, T. inermis, according to Nemoto,
is species-specific. It seems to us that the larger the crustaceans, the
larger the size of the school. The largest schools, doubtless, are those
of E. superba; the concentration in the school is up to 100 kq/m3 (Marr,
1962; Nemoto, 1968). School formation in euphausiids is an active process
(Zelickman, 1960a, 1961b; Zelickman, 1961), probably resulting from a
combination of causes. We consider school formation in euphausiids to
be a characteristic primarily of phytophages, which cast their spawn into
the water; the young of these species begin to feed on phytoplankton in
the first calyptopis stage. School formation occurs in the regions where
the young will feed; in any case, during the spring and summer biologic
season in the Arctic and, apparently, Antarctic waters, schools are always

33

observed in areas with abundant plankton. It is not clear whether true
schooling occurs in euphausiids with predatory and mixed feeding habits.
Large aggregations are occasionally formed by Thysanoessa longicaudata
(Forsyth, Jones, 1956) , Euphausia diomedae and Stylocheiron abbreviatum
(Roger, 1974), but these data, based on extended catches, do not prove that
what was encountered was a true school, rather than a simple accumulation
with an unknown degree of integration.

Schooling is seen in most massive species of mysids (Mauchline, 1971).
Schools of Leptomysis linguura may be quite permanent and remain almost every
day in the same place. Schooling is observed in _L. mediterranea and Siriella
armata only in the day, particularly if there is a gradient of illumination.
Schools of !L. 1 inguura simultaneously contain individuals with different
photoactivation (Macquart-Moul in, 1971, 1973; Macquart-Moul in , Patriti,
1966). Schools of Mysidium gracile find shelter among the spines of the
sea urchin diadema antillarum (Emery, 1968). Fish never capture mysids
from these schools.

The characteristics of schooling and the behavior of mysids in a
school agree in basic features among the various species (Zelickman,
1974; Zelickman, 1975); the behavior of mysids and euphausiids is similar
to the behavior of fish in a school as described by Radakov (1972). The
orientation of individuals in a school and observation of spacing are
apparently maintained by the optometer and kinesthetic systems of orienta-
tion. The forms of integration of groups of mysids and other crustaceans
which have been observed permit their behavior to be interpreted as an
integral, complex reaction of the organisms, rather than simply an ensemble
of kineses and taxes. The mechanism of orientation of the mysids is probably
governed by the level of illumination, the position of the light source, its
polarity and, possibly, spectral characteristics; no less important is
distance perception--the location of fluctuating movements of the water, at
least for species which school in darkness. It is possible that various
reception systems function simultaneously, with an overall coordinator.
There is e^^ery reason to assume, for example, synergy of receptor perceptions
in hermit crabs (Hazlett, 1970).

We must not consider the heterogeneity of physical characteristics of
the aquatic medium the primary cause of the high degree of organization of
groups of animals, particularly crustaceans, both in nature and under
experimental conditions. The adaptive capabilities of schooling behavior
among crustaceans can be compared to selective advantages which arise upon
schooling of fish. These advantages must entail evolutionary optimization
of the collective reactions of animals favorable to the population. These
collective reactions are most useful to massive species subject to predation,
and are also necessary in situations requiring movement of entire populations,
e.g., spawning migrations. What are the parameters which must be optimized
in order to preserve a population? In this case, one of the semiquantitative
abstract models (Vine, 1971) of differentiation of the hunting behavior of a
"visual predator" as a function of the type of distribution of prey seems
applicable. This model considers a situation in which the prey, of identical
size, is attacked by a predator, which is located either within or outside

34

the population of prey and scans the visible space in order to locate its
prey. The strategy of the prey should be optimized with respect to a
number of criteria--maximum individual and group safety, minimum probability
of pursuit, maximization of the time required for detection and capture.
Vine showed that in this situation, it is most favorable to the prey to
be evenly distributed in a circle; within a circle, the prey should form
an arc so that the head of the rearmost individual is directed toward
the tail of the foremost individual. The greatest individual safety will
be achieved by individuals in an ordered pattern around the periphery of
a sector or at the center of a chain. Schools which can observe in all
directions see predators most easily and can restructure themselves most
quickly. The "nose to tail" position is favorable for the group of prey
as a whole. Some of the advantages of schooling are also gained by each
individual, e.g., when the predator hunts by individual capture of prey, it
is favorable to increase the size of the school (minimize the size of the
target prey). The adaptive results of schooling following from the geometry
of the constructions of Vine, agree with field observations (J. A. Allen,
1968; Delia Crose, Holthius, 1965; Herrnkind et al . , 1973; Losse, Merrett,
1971; Emery, 1968) and experiments (Steven, 1961; Clutter. 1969; Zelickman,
1974, etc.). Of course, other principles of configuration and geometry of
the school are possible, e.g., when interacting with a prey, orientation
by chemoreceptors, during sexual interactions, behavioral interactions,
etc. However, a given geometry of spatial organization of individuals of
the same species as a method of decreasing predation is doubtless one of the
most probable adaptive structures of this behavior.

In those cases when many prey individuals are absorbed at the same time,
e.g., when whales feed on swarms of Euphausia superba, the train of argument
presented above might seem inapplicable. However, one should recall that
swarms of E. superba vary greatly in size. The mosaic-like distribution of
the prey and the rapidity of restructuring of swarms fatigue the predator
and, probably, make the search for the prey much more difficult.

Thus, the types of nontrophic connection in a community have as many
aspects as the competition for food, and are based on the purposes which
are common for all bonds in populations: spatial and reproductive isolation,
elimination of nonviable genomes from the breeding stock, weakening (by
ritual ization, pheromone regulation, etc.) of intraspecies and interspecies
interactions which are too active. Essentially, the etiologic bonds are
equivalent to communication lines among individuals of the same or different
ages, one or both sexes, between generations and populations. Intraspecific
and interspecific communications have evolved from a single-bit information
system to a multiple-bit system (Sebeok, 1969). In the sea, this path is the
same as on land. From external metabolites as the simplest carriers of
information, species go over to the utilization of other channels for
information transmission--the vibrotactile, visual and acoustical channels.
The information capacity of the etiologic signaling also increases; in
hermit crabs, lobsters and crabs it may be as great as in social insects
and birds (Hazlett, Bossert, 1965; Hazlett, 1972b; Hazlett, Estabrook, 1974).
The development of the ability to recognize patterns leads, on the one hand,
to greater individualization and complication of etograms and, on the other

35

hand, to the development of schooling behavior as a system of adaptation
of the population as a whole. The complication of the etiologic integrative
elements observed in any community of free-living organisms, like the
strengthening of their significance in a phylogenetic sequence, is a
process which occurs in parallel to the creation of the second signal
systen: in man.

36

CHAPTER II. PELAGIC COMMUNITIES AND THEIR STRUCTURAL
AND FUNCTIONAL CHARACTERISTICS

1 . Trophic Relationships in the Pelagic Zone

(M. E. Vinogradov, N. V. Parin, A. G. Timonin)

Primary sources of matter and energy. The trophic relationships in
the pelagic zone of the ocean, in spite of their great importance for an
understanding of the functioning of communities, have been quite insuffi-
ciently studied. Even such a basic problem as the primary sources of
incoming organic matter (energy) entering the food chain of the communities
which; in the final analysis, determines their total productivity,
functioning and structure, is still a subject of lively debate.

The primary organic matter in the pelagic zone is formed by the
photosynthetic activity of phytoplankton. It is thought that the entire
food pyramid is constructed on this basis. The flow of energy passes
through the phytoplankton to the herbivorous zooplankton, then to the
carnivorous plankton and nekton (Fig. la). However, attempts at quantitative
estimation of the energy flow and energy balance of the various trophic
levels have shown that over broad expanses of water in the oligotrophic
regions of the tropical ocean, this path cannot support the energy demands
for existence of the communities. At least in these regions, obviously,
another path of arrival of energy is no less 1mportant--through autochthonous
and al lochthonous dissolved organic matter to bacteria, protozoa, then
filtering and predaceous invertebrates (Fig. lb). It is assumed here
(Sorokin, 1971a) that the dissolved organic matter is formed in excess in the
highly productive cold regions of the ocean, descends together with the
descending flows of water into the deep layers where, due to the low tem-
perature, its decomposition is retarded, then returns to the surface in
the equatorial regions in the areas of quasi-stationary upwelling of water
where, at the high temperatures reached in the surface layers, it becomes
available for bacterial destruction. Thus, the bacteria in these tropic
communities act as local "producers." Yu. I. Sorokin (1971a) believes
that the bacterial path of inclusion of organic matter in the food chain
in tropical communities is equal. In terms of energy flux, to the classical
phytoplankton path, or even exceeds it. This high evaluation is not agreed
with by all (Steemann Nielsen, 1972; Banse, 1974), but, nevertheless, the
significance of the role of arrival of energy in the community through
dissolved organic matter and bacterioplankton is obvious.

The trophic network of the community. The distribution of matter and
energy among trophic groups in the community follows a complex network of
trophic connections. Connections at the higher trophic levels may be
comparatively easily traced by examining the contents of the guts of

37

w

w

Light-x^ ,

9 ^'^t^ ^^s=4>^^

/

Uutrierics

f

?/ Phytoplankton

a

Zooplankto"

B

t > :s'C

i'i" ^ '«?"- -^

Dissolved Y^ prntn^o

organic

matter

Zooplankton

■lutr lerit'^

Fig. 1 Paths of arrival of organic matter (energy) into the food chain
of communities. A, "pasture" food chain; B. "detrital" food chain.

predators. It is more difficult to evaluate the food chains of the smaller
animals at the lower levels--those which suck out only the contents of
the bodies of their prey, or which feed on small organisms without skeletons
(e.g., protozoa) or bacteria. Analysis of the food's remains in their food
lump is not sufficient to indicate the spectrum of their nutrition. In
this case, other methods must be used for the investigation--study of the
morphologic-functional peculiarities of the feeding apparatus, experimental
feeding using various food labeled with C^'^, direct observation under
experimental conditions of the nature and intensity of feeding.

sh a number of trophic
phytoplankton); phytophagous
crustaceans, nnollusks, some
us animal s--first-order
aths, amphipods, etc.); larger,
ophagous fish, baleen whales);
d cephalopods, marine birds
edators--medium-sized
sharks and the toothed whales,
even in extreme cases, the
n (Parin, 1968, 1970). Upon
igher level, an average of

Within the food network, we can distingui
levels: primary producers of organic matter (
pelagic animals: many copepos and euphausiid
(few) fish; predators which feed on phytophago
predators (many copepods crustaceans, chaetogn
second-order predators (decapods, small plankt
third-order predators--basical ly small fish an
and reptiles; fourth-order and higher-order pr
and large bony fish (tuna, alepisauri, etc.).
The total number of trophic levels may reach s
four upper levels consisting entirely of nekto
transition from each lower level to the next h
about 90% of the energy is lost.

Since the food connections in a community are quite complex and
variable, the distinction of trophic levels is quite arbitrary. Actually,
the diet of many predaceous forms at the lower levels may include phyto-
plankton; second and third-order predators eat both predaceous and phyto-
phagous animals; some squids and predaceous fish, occupying the upper
levels of the trophic network (particularly the bugeye and yellowfin tuna)
act as euryphages, eating anything of the appropriate size--from euphausiids
to squid and fish. Depending on the presence or abundance of any of these
items, their significance as a part of the diet may change significantly.

In spite of the instability of the separation of individual trophic
levels in a community, their number, i.e., the length of the food chain,
may differ significantly from community to community. This is determined,

38

in the final analysis, by the varying stability of the communities which,
according to MacArthur (1955), increases as the number of links in the
food chain increases. High stability of a community, according to
Margalef (1968), allows it to exist with a lower specific quantity of
energy entering the system, i.e., with more limited food resources.

In the oligotrophic tropical or deep-water communities, the number
of trophic levels is high, while in regions with a high level of primary
production, the food chains of the communities are very short. For example,
in the ultraeutrophic waters of the Peruvian coastal upwelling, the trophic
chain of the pelagic zone community consists of only two main links: the
phytoplankton and the anchovies. The presence of mass species of fish
feeding directly on the phytoplankton is also characteristic for other
subtropical, highly productive upwellings. During certain periods,
phytoplankton dominates in the food of Sardinella aurita in the upwelling
off northwest Africa, for Sardinops melanosticta and Engraul is japonicus
off the Pacific coast of Japan, and for Sardinops caerulea in the Oregon
upwelling, etc.

The trophic structure of communities in various climatic zones. The
basic differences between subpolar and tropical regions of the ocean is
that in the former there are great seasonal changes in the environmental
conditions--the intensity of solar radiation, temperature, stratification
of surface waters--whereas in the tropics, these factors change little.
These planetary distinctions, in the final analysis, also determine the
difference in the trophic structure of communities.

The trophic systems of communities in cold water and temperate to
cold water regions are adapted to achieve the most effective utilization
of the comparatively brief but clearly expressed spring maximum in biomass
of phytoplankton, whereas in open regions in the tropical ocean, the
system is adapted to achieve most complete utilization of the relatively
low, but little changing level of production of phytoplankton throughout
the year.

In Arctic, boreal and Antarctic regions, the main producers are the
diatoms. Their primary consumers are copepods, euphausiids and (in certain
regions) pteropod mollusks. Zooplankton is consumed by coelenterates ,
carnivorous copepods, hyperiids, chaetognaths , baleen whales and plankto-
phagous fish. These fish, in turn, are eaten by predatory fish and squids
(Fig. 2, A).

In the open regions of the ocean at low latitudes, the picture of
trophic interactions in a community is much more complex (Fig. 2. B). The
primary sources of food are phytoplankton and bacteria. In addition to
the small phytophagous plankton, macroplanktonic predators are very
important, serving as the primary food of planktophagous fish which, in
turn, are eaten by larger predaceous fish, while these, in turn, are eaten
by tuna and sharks (Parin, 1968, King, Ikehara, 1956, etc.).

39

Diatoms

Bacteria

Herbivores: copepoda, cuphausiids, I ''
pteropoda

Ji^

Plonktonic zoophages: coelenterata,
copepoda, chaetognatha, hyperiidae,
euphausiids

_iU-

Protozoa

)

Ba

leen ;;halesH~^A

B

Planktophagic fish: herring, cape-
lin, saury, pollock anchovy, etc.

V Predaceous fish, squid, salmon, cod, A
^ etc. /

Phytoplankton

I — ^ Bacteric
I //

A-

Herbivorous plankton: copepoda,
salps, euphausiids, pteropoda

I r

±-

^r^ Protozc:

V

.q

:/,

Small predaceous zooplankton: cope-
poda, chaetognaths, polychaetes,
coelenterata

/

/

/

^

Predaceous plankton and micronekton:
shrimp, coelenterata, sr.all fish

Small nektonic predators: squid,
medium-sized fish, etc.

A.

Large nektonic predators: tuna,
dorado, swordfish, sharks, etc.

T

Largest nektonic predators: great
while shark (cnrjarodon) , etc.

Fig. 2. Flow charts of basic food chains in polar and temperate (A)
and tropical (B) areas of the ocean.

40

However, in the more productive regions of the lower latitudes in
quasi-stable upwelling zones, the trophic structure of the community is
significantly different: The food chain consists of a few links, sometimes
even a smaller number than in the productive regions in the higher latitudes.
These communities, with their short food chains and rigidly determined
direction of the flow of matter and energy, yield extremely high production
of the final links (fish), but their stability is quite low. The communi-
ties cannot react flexibly to significant changes in production of one
of the links in the chain and, for example, a sudden decrease in production
of the first link (phytoplankton) leads to truly catastrophic results.
Examples include the well-known periodic disruption of the structure of
the ecosystem of the Peruvian upwelling during "El Nino," causing catastrophic
decreases in the catches of anchovy, deaths of hundreds of thousands of
fish-eating birds, etc.

The communities of productive regions in the higher latitudes have
special adaptations to the annual (and, of course, seasonal) fluctuations
in the production of phytoplankton and therefore, even with significant
changes in the population of the primary producers or consumers from year
to year, catastrophic disruptions of their structure do not occur.

Changes in food interactions during development of communities. Marine
pelagic communities, like sea-floor communities or continental communities,
undergo significant structural changes from the moment of their formation
until they reach the mature stage. The initial stages in the formation of
communities occur with mineral forms of nutrients present in the photic
layer. In this stage, the processes of accumulation of energy in the
community prevail over processes of its dissipation.

As an ecosystem develops, the total content of nutrients in the
water decreases to the extent that it causes a decrease in the biomass of
phytoplankton and a change in its dimensional and systematic composition.
Due to the different rates of maturation and achievement of maximum numbers
of different trophic groups in the community, the entire trophic structure
changes.

As the community matures, it is gradually carried downstream. There-
fore, the time difference in achievement of the maximum development by the
different trophic elements of the community leads to a shift in space, as
well. Many observations in tropical regions in the Pacific and Indian
Oceans have shown that the zones of maximum population of phytophages
are usually long, narrow belts, crossing the oceans along lines of divergence,
This, for example, is the distribution of Undinula darwini , the maximum of
which in the Indian Ocean is found at the divergence at the boundary of the
southern equatorial current and the equatorial countercurrent , and in the
Pacific Ocean at the equatorial divergence (Vinogradov, Voronina, 1962, 1954).

The maximum population of mature carnivorous surface-dwelling copepods
(Euchaeta , etc.), in contrast to the phytophages, is located parallel to
the divergence, but displaced from it by 60-90 miles. Furthermore, in
the Pacific Ocean, the maximum population of mature \]_. darwini and

41

Fig. 3. Diagram of distribution
of various trophic links of plank-
ton and nekton in the zone of
divergence and convergence near the
equator. 1, phytoplankton;

2, phytophagous zooplankton;

3, predaceous zooplankton;

4, large fish.

Rhincalanus cornutus in the rich equaLo; lal divergence is observed in two
narrow strips along 0°30"-l°N and S latitude. Thus, as they grow, the
crustaceans, which develop in the "juvenile" water, as it diverges, are
carried north and south by the meridional components of the currents. The
maximum of sexually mature individuals, however, is not shifted as far
from the center as is the maximum of predaceous copepoda.

Naturally, the shift is greater, the longer the time of maturation of
a species, the greater the speed of the current or the higher the position
of the organism in the food chain. Therefore, accumulations of macroplankton
and the large fish which feed on it, as a rule, are located to the side of
a zone of divergence and usually fall along the nearest convergence, beyond
which they cannot be carried by the meridional component of the equatorial
currents (Fig. 3). In the equatorial zone, it is at these convergences
that we observe the greatest accumulation of flying fish (Parin, 1968).

A. G. Timonin (1971) used the example of the tropical regions of
the Indian Ocean to study the changes of the roles of various trophic groups,
trophic and specific diversity in communities in regions with varying
intensity of upwelling, i.e., varying degree of maturity of the population
of the community (see Figs. 1, 2). The young communities in regions of
intensive upwelling are characterized by high plankton biomass, low trophic
and specific diversity, resulting from an increase in the total quantity
of zooplankton due to domination by a few species. Filter feeders predominate
(up to 58%), among these--coarse filter feeders such as Eucalanus attenuatus,
E. subtenuis and Rhincalanus cornutus, which make up as much as 45% of
the total biomass and 85% of the biomass of filter feeders. Predators
represent 20-25% of the total mass of zooplankton. Where the water ascends
upward more slowly, the total biomass of zooplankton is lower. Specific
diversity increases, since the degree of domination by individual species
decreases. The trophic structure becomes more diverse, but filter feeders
still predominate, representing about 40% of the total biomass. The fraction
of predators increases to 30-35%. Mature communities, in regions where

42

upwelling is absent or where the water is descending, have low plankton
biomass, high specific diversity, and weakly expressed domination of
species. The trophic structure reaches almost its maximum possible diversity.
Filter feeders amount to about 20-30% of the total biomass, and more than
half of them are fine-filter feeders. The total quantity of predators
increases to 45%. Analogously, in mesopelagic macroplankton in the mature
communities of the central and western equatorial Pacific, the biomass is
less, the specific variety significantly greater, than in the more juvenile
communities of the eastern Pacific (Parin, 1976).

Factors which greatly shade the typical picture of distribution of
trophic groups come into play in the higher levels of a trophic system.
This results to a great extent from the fact that in the macroplankton and
nekton of the open ocean, a large portion of the flow of energy is directed
downward and beginning as low as the second or third level of consumers, a
significant fraction of the total biomass is accounted for not by
surface-dwelling, but by deeper dwelling, primarily mesopelagic, animals.
The transformation of this flow on its path down into the depths has not
been sufficiently studied, but subsurface currents apparently are quite
significant in the redistribution of animals. Therefore, the spatial
distribution of oceanic tuna, which make up the basis of an important
industry, and of the toothed whales (particularly the sperm whales), feeding
on mesopelagic fish and squid, cannot always be given an effective causal
explanation from the point of view we are now considering.

Change in trophic structure of communities with depth. The change
in the role of various trophic groups of mesoplankton with increasing
depth will be analyzed on the example of the region of the Pacific Ocean
near the Kuril Islands, since we have representative quantitative data on
the vertical distribution of the entire mass of plankton and its basic
taxonomic groups for this area (Table 1, Fig. 4).

The planktonic community, rich in phytoplankton, in the upper portion
of the euphotic zone, is dominated by phytophagous filter feeders. In
the lower levels of the euphotic zone, in the cold intermediate layer
(100-200 m), the significance of predaceous species (primarily Sagitta
elegans) , feeding on animals from the surface layer, increases rapidly.
The significance of filter feeders decreases, although it remains rather
high as far down as 500-750 m. In the 500-1000 m layer, the significance
of the euryphages increases, due to the development of a rather large number
of radiolaria from the families Aulacanthidae and Aulosphaeridae at these
depths, serving as a significant component of the diet of the euryphages,
and also acting as predators of the copepods. Below 500-1000 m, the signifi-
cance of the filter feeders decreases rapidly. The quantity of specific
deep-water filter feeders is "jery small. The interzonal filter feeders,
present in comparatively large numbers (primarily the copepods Calanus
cristatus and C^. plumchrus) , feed in the producing zone and, apparently, do
not feed in the deeper waters. Ignoring the interzonal phytophages, in
the 1500-3000 m layer, the plankton consists 60-80% of zoophagous forms,
primarily catching zoophages. Deeper than 3000-4000 m, given the '^ery low
plankton biomass and its great dispersion, predation, even passive
predation, is apparently not energetically expedient, and the significance
of zoophagous forms is greatly decreased. Euryphages move into first

43

Table 1. Change in significance of basic trophic groups of mesoplankton
in Kuril region of the Pacific Ocean with depth in the summer of 1966
(% of total mass of mesoplankton in each level, ignoring interzonal filter
feeders which do not feed at the depth where caught--after Vinogradov, 1968).

Depth, m

Filter feeders

(phytophages
and detrito-
phages)

Catchers

(zoophages--

predators and

Euryphages

scavengers)*

n

4

33

8

51

5

27

17

25

16

46

31

47

29

66

16

74

13

86

8

6

22

32

46

15

50

9

51

1

37

14

31

0-50

50-100

100-200

200-300

300-500

500-750

750-1000

1000-1500

1500-2000

2000-2500

2500-3000

3000-4000

4000-5000

5000-6000

6000-7000

>7000

83

57

40

53

50

9

11

4

2

3

5

3

3

1

1

4

*The biomass of predators is low, since we do not include the weight
of coelenterates or of large cephalopods and fish which are not easily caught

in plankton nets,

place, being able to utilize the greatest variety of food--living organisms,
their remains and fecal matter, raining down from the overlying layers.

At 4000-6000 m depth, the significance of phytophages increases again,
due to the presence of mysids of the genus Boreomysis. These mysids feed
on phytoplankton in the surface layers, then descend to the deeper layers,
where there are practically no predators, and the probability of their
being eaten is greatly reduced. Studies performed on board the VITYAZ
have shown that groups of Boreomysis incisa with stomachs packed with
fragments of diatoms and Tintinoidea, are constantly observed at a depth
of 4000-6000 m, sometimes slightly higher or lower (Vinogradov, 1970a).
This indicates that there is regular, rapid transport of phytoplankton
through a tremendous mass of water and emphasizes once more the importance
of vertical migration in the transportation of organic matter from the
productive zone to the depths of the ocean. Almost the entire mass of
copepods at these depths consists of euryphages. Deeper than 6000 m, the

44

^^^ p ."5 eg

!0D %

Fij. 4. Change in role of various trophic
groups in the plankton of the northwestern
Pacific with depth. 1, Filter feeders--
phytophages and detritophages ; la, filter
feeder-phytophages which feed in the
surface layers and do not feed at the
depth where caught; 2, zoophagous species--
predators and scavengers; 3, euryphages;
4, radiolaria and their remains and other
groups not considered above.

plankton is dominated by euryphages, and only in the benthic layers does
a significant Quantity of zoophagous polychaetes and amphipods appear,
probably associated with the floor.

In contrast to the eutrophic boreal regions, in the oligotrophic
tropical regions among the most important group of plankton--the copepods--
in the upper 100 meter layer zoophages already predominate, while the
significance of filter feeders decreases from 40* in the 0-50 m layer to
15X in the 200-500 m layer. Beginning in the mesopelagic zone, euryphages
predominate, continuing to dominate the entire column of water: in the
2000-4000 m layer they make up 76X of the mass of copepods, below 4000 m--
94% (Arashkevich, 1972).

In both of the areas in question, the relationship of various trophic
groups changes rather similarly as we move vertically downward. However,
in the boreal area, predators play a significant role in the plankton down
to 3000-4000 m depth, whereas in the tropical area, less rich in food,
their role is reduced to nil by a depth of 2000 m. The zoophagous macro-
plankton is correspondingly distributed: In the boreal waters, a compara-
tively high concentration of zoophagous forms is observed down to 3000 m,
in the tropics--down to 1500-2000 m.

Thus, based on the relationship of the various trophic groups in the
pelagic zone, we can distinguish rather clearly different layers, approxi-
mately corresponding to the surface, moderately deep and abyssal distribu-
tion of the planktonic biomass (Vinogradov, 1968). The superficial
layer extends down to 100 (or 200) m and is characterized by clear
domination or predominance of fil ter-phytophages. Then, from 200-500

45

(750) m is an intermediate layer without clear domination of representa-
tives of any one feeding group. At depths from 750-1000 m to 3000 m in
the tropics, zoophages play a significant, usually dominant, role.
Deeper, euryphages dominate.

Basic trophic complexes of macroplankton and nekton at various depths.
The vertical zones of the oceanic pelagic zone correspond to the trophic
complexes of macroplanktonic and nektonic organisms occupying the higher
levels of the food chain (Parin, 1970, 1971; Borodulina, 1974).

The epipelaqic complex consists of (holoepipelagic) crustaceans,
constantly inhabiting this biotope (euphausi ids , less frequently shrimp),
cephalopods, fish, sea snakes and chelonia and many whales, as well as
the interzonal animals which rise to the surface at night to feed (nycto-
epipelagic species). The second level predator niche here is occupied
primarily by macroplanktonic organisms and relatively small fish (in the
higher latitudes, until recently baleen whales were extremely important);
at higher levels, only nekton are represented (large fish, dolphins, etc.).

An independent trophic complex can be distinguished in the tropical
area in the boundary layer between the epipelagic and mesopelagic zone,
at a depth of 100-300 m. This complex combines second and third level
planktophages, constantly present at these depths (certain euphausiids
and hyperiids, juvenile squids and fish, mature fish from the families
Sternoptychidae, Scopelarchidae, etc.) or numerous euphausiids, shrimp
and myctophids, migrating here at night from the mesopelagic zone to
feed. All these animals, including the interzonal migrants, serve as
food for such nektonic predators as fish from the families Paralepididae,
Bramidae, Gempylidae and a number of species of squid from the families
Ommastrephidae and Onychoteuthidae, which are themselves eaten by the
alepisaurs, large ("level") tuna and marlins, sharks and bottlenose
whales (but not'the sperm whale). All of these, except for the alepisaurs,
are genetically related to the epipelagic area (which is indicated in
particular by the fact that smaller species of tuna and the juveniles
of larger tuna and marlins inhabit the surface levels), and their departure
from the upper layers is energetically justified by the richer food avail-
able in the boundary area between the epipelagic and mesopelagic biotopes.
The epipelagic and interzonal organisms rarely form a part of the food of
these predators (Fig. 5), since they feed in this layer during the daylight.

In the mesopelagic zone itself, coexist two trophic complexes--the
stable complex, consisting of nonmigrating or short-range migrating animals,
and the migrating ("strata!") complex, including organisms which perform
daily vertical movements as a part of the migrating sonic scattering
layers (SSL). Both complexes consist primarily of macroplanktonic (or
micronektonic) crustaceans, cephalopods and fish, primarily third or fourth
level predators; the true nektons are very scarce in the mesopelagic zone,
the most important of them being the sperm whales, which feed in this layer.

The special trophic complexes of the deep layers of the oceanic pelagic
zone--the bathypelagic and abyssopelagic zones--are combined by their

46

SalaSnii

Fig. 5. Primary trophic connections of macroplankton and nekton in the
tropic oceanic pelagic zone, on the example of the diet of the bluefin (1)
and yellowfin (2) tunas: 1-3, food connections of the tunas: 1, most
important {>10% of arbitrary re-established weight of diet); 2, less
important (5-10%); 3, still less important (<5%); 4, food connections with
other nektonic and macroplanktonic organisms (according to Borodulina,
1974).

47

adaptation to the scarce food resources of these zones. The animals
which make them up have characteristically adapted to reduced energy
expenditures, manifested as a transition to a passive mode of life. For
this reason, there are no nektonic animals in the bathypelagic or, par-
ticularly, the abyssopelagic zone, and even the largest inhabitants of
these biotopes--and some fish (the angler fishes Himantolophus and Ceratias)
and squids (Mesonychoteuthis) reach a meter or more in length--must be
considered macroplankton.

The primary trophic complexes of the macroplanktonic and nektonic
animals in the pelagic zone of the ocean, though they are clearly separated,
are still interconnected to some extent and form only individual sections
of the single trophic network. The "contact" is particularly clearly seen
in the complex at the upper boundary of the primary thermocline, where
elements of the epipelagic and mesopelagic complexes come in contact and
conditions are created for a significant concentration of food resources
for the large nektonic predators.

48

2. Communities of the Arctic Waters.
(E. A. Zelickman)

The cyclical nature of the functioning, i.e., the presence of popu-
lation waves in the Arctic ecosystem, is a general property of this system,
reflected in the formation of all production characteristics. It results
from the light limitation of photosynthesis. In an ecosystem which must
function in a fluctuating mode, selection fixes only those hereditary
changes in organisms which correspond to a broad reaction norm. Compensa-
tory paths of stabilizing selection are primarily limited to multiplication
(Shmal 'gauzen, 1968). With a brief season of abundant food, selection
goes to higher fertility, and selective elimination may be directed toward
various phases of ontogenesis. In this case, the reproductive potential of
the species, as a rule, which is not realized in the Arctic community, may
manifest itself as compensation. Therefore, in the Arctic community, only
"opportunistic species" with high ecologic valence: high numbers of
population, flexible reaction to unfavorable changes in the environment,
high growth rate of the population under favorable conditions and high
mortality, can blossom. The dominant species of this profile in the
Arctic community can be compared (Margalef, 1968) to a thermostat, consuming
a great deal of energy while acting as a regulator. This type of "equipment"
withstands extreme conditions, converting fluctuations in the environment
to the benefit of the system. Just what are the means of this damping?

If the production of plankton communities is interpreted (Cushing,
1959a, b, 1969) as a result of contradictory relationships among populations,
the course of the curve of creation of products is determined by the time
interval between the peak of blooming of the phytoplankton and the moment
of greatest intensity of consumption. Arctic and boreal communities differ
essentially only in the length of this interval, proportional to the distance
from the Pole. In other words, an Arctic community as a whole has its own
unique "system time," and in each season the community must adapt to this
system time, synchronizing its state with the time. The balance between
producents and consumers in this interpretation is a characteristic which
is more temporal than quantitative. Therefore, the synchronization of the
processes of creation of biomass and its destruction at the next trophic
level is one of the leading trends in selection in the Arctic ecosystem.
Idioadaptation at the species level should support temporal contact and the
normal sequence of the cycles, while the equilibrium between production and
consumption is checked by the entire system of mechanisms inherent in the
community as a whole. One of the indirect mechanisms synchronizing the
system is the high P/B coefficient (for values of indicators, see
Kamshilov, 1955, 1958; Timokhina, 1968, 1972), corresponding to the
seasonal asymmetry of the curve of food resources.

The obligatory pulsation in the status of the community may be a
specific method of stabilization of the system, but not a method of its
disruption. The fluctuation processes in the Arctic encompass the entire

49

hierarchy of trophic levels in a definite sequence, but with varying
intensity. However, in the annual cycle, the production of the community
remains relatively stable, since its basic parameters (species composition,
numbers, biomass) do not go beyond a certain framework.

The population waves, as an attribute of all life cycles in the
Arctic, facilitate the appearance of new genotypes in the evolutionary
arena (Huxley, 1942). The fluctuating mode also influences the boundaries
of the area of distribution of Arctic and Arctic-boreal species, which
alter their "case" with periodic changes of abiotic conditions.

The oscillating type of dynamics predetermines the resiliency of
the structure of the populations and the strong intraspecies mutual
dependence. The Arctic ecosystem, which is self-reproducing in the
oscillating mode, to some extent refutes the thesis of the incompatibility
of maximum productivity of a community with the status of its highest
stability. If we look upon constancy of relationships of biomass of
species in a community as one criterion of stability, this constancy is
retained on the average over the annual cycle (see below). Obviously, it
is more correct to evaluate, in this case, oscillations in numbers as a
manifestation of stability (Preston, 1959): They make the community less
vulnerable. From the standpoint of evolutionary advantages, this form of
stability can be considered most adequate for biological progress, as
understood by A. N. Severtsov.

2.1 . Comparison of the Arctic Ecosystem with Other Productive Systems

The concept of "system time" allows us to note the deep structural and
functional similarity between the ecosystems of the different productive
zones and their particular blocks. For example, the "behavior" of marine
and fresh-water Arctic communities is similar (Dodson, 1975; Tash, Armitage,
1967).

The shelf-neritic communities of various latitudes, like the Arctic
community, are the arenas of seasonal "demographic explosions." The
spatial distribution of phytophages and predators in the area of the polar
fronts of the Norwegian and Greenland seas (Gruzov, 1963; Pavshtiks, 1972)
is similar to that in the region of the West African upwelling (Bainbridge,
1972): In both cases at the "line" of the front and in the zone of maximum
upwelling, phytophages predominate, with predators predominating around
the periphery. There are also analogies in the systems of adaptations. We
need but recall the similarity of the life cycles and life forms of
Arctic-boreal and neritic euphausiids as a counterweight to the oceanic
forms, regardless of their latitudinal distribution (Zelickman, 1968a;
Gilfillan, 1972). Convergent adaptations are seen in the upper boreal
Calanus finmarchicus and lower boreal C. carinatus, e.g., the winter
descent of the stage V copepodites (Bainbridge, 1972).

The small variety of life forms in the Arctic ecosystem is compensated
for by the intensive intraspecies divergences. Within the framework of the
Arctic ecosystem, sympatric radiation occurs among the dominating species
Calanus, Pseudocalanus , Limnocalanus , Oithona , Parathemisto, Mysis and

50

Thysanoessa. The great number of microzooplanktonic predators, along
with the phytophages and the great specific weight of carnivorous feeding,
are characteristic for the epiplankton of all productive zones. For
example, in the neritic waters of the Barents Sea, in the upper 30 centimeter
layer, an asymmetrical quantity of Oithona, Sagitta and Pseudocalanus of all
ages is observed, as well as Cladocera, Fri till aria and Oicopleura
(Shuvalov et al., 1974). According to our observations, the number of these
animals in May-September (per unit volume) in the 0-30 cm layer is 3-4 orders
of magnitude greater than in the 0-10 m layer. This concentration of
predators and phytophages in the narrow surface layer indicates the precise
feeding differentiation of the massive species.

Although in the Arctic community, the biomass of zooplankton in the
tremendous water area of the neritic and shelf regions is also higher than
in the oceanic waters, the "neritic underutilized phytoplankton," of which
A. K. Heinrich wrote (1961a, b, 1962), apparently does not exist. In the
Barents Sea, it is in these neritic waters that phytoplankton is consumed
earliest and most completely (Roukhiyaynen. 1960). Were this underutili-
zation real, the dominant phytophages would not eat animal food, either in
winter or, particularly, in the summer. In nature, Calanus finmarchicus
supplements its protein supply by predation, both summer and winter (Adams,
Steele, 1966), although in the laboratory, this species can survive for
long periods of time on a diet of algae alone. On the shelf of the
epicontinental seas of the Arctic, for example near Novaya Zemlya (Zelickman,
Golovkin, 1972), the great biomass of zooplankton is formed where the
phytoplankton is richest. The excess phytoplankton, i.e., imbalance, is
nonexistent: The disproportion which arises is eliminated by changes in
the population of the massive species and in the number of their generations.
In other words, the temporary "excess" is regulated by the consumers them-
selves. Thus, with low concentrations of algae cells, the rate of filtration
of the Copepoda decreases, and the level of nutrition supports only the
minimum vital activity. The low rate of consumption allows the phytoplankton
to increase in number, after which it is immediately utilized by the Copepoda
to increase their own egg production (Adams, Steele, 1966; Poulet, 1974).

2.2. Spatial and Morphophysiologic Differentiation of Organisms

as a Form of Transformation of Fluctuations within the Arctic
Ecosystem

The flexibility, "elasticity" of the system, given the relatively low
number of life forms, is achieved, particularly, by redistribution of
"energy clusters" within the community both in time and in space. The
space and time segregation of massive species and their hemipopulations is
clearly expressed. The capability of organisms to hold themselves in a
predetermined water mass reinforces this heterogeneity, guaranteeing the
species and their hemipopulations synchronous coexistence. During the
polar day, the intrapopulation spatial differentiation is primarily ex-
pressed in the horizontal plane. One example can be found in the local
schools and zones of abundance of C. finmarchicus , Thysanoessa inermis, and
]_. raschii (Zelickman, 1958, 1961by. In the Barents Sea, the main body
of zone of abundance of Calanus, Pseudocalanus and euphausiids, as well as
their young in spite of seasonal movements, are always distributed
throughout the depths. The euphausiids of the present and previous year
are distributed horizontally.

51

The role of ontogenetic migrations in the formation of spatial
heterogeneity under the conditions of the Arctic ecosystem increases due
to the interruption (or decrease in the amplitude) of diurnal vertical
migrations during the polar day. It is the ontogenetic descent which
determines the replacement of the spring and summer oceanic complex of
species by the summer and fall neritic complex, changing the nature of the
plankton diet of the fish. In many cases, the ontogenetic migrations also
result in temporary intraspecies segregation. For example, in Calanus
glacial is in the fjords of Greenland (McLellan, 1957), the rise of VI
copepodites to the surface is synchronized with the phytoplankton peak in
the internal and external areas of the fjords, so that the stage I
copepodites are universally supplied with food. Therefore, the males with
spermatophores do not appear simultaneously in the various subpopulations.

There are various means of achieving spatial separation. One of these
is the aggregation of distribution observed in any community. When there
is a '^ery high numerical strength of species, particularly in a glacial-
neritic system, clear effects of aggregation are observed. In the shallow
Arctic bays (e.g., in the Cheshskaya Bay of the Barents Sea), a multitude
of ephemeral "microcommunities" are observed. They are rather permanently
isolated from each other due to the shallow turbulent currents and complex
density stratification. Over a distance of a half mile, the plankton might
differ by 5 or 5 orders of magnitude as to number, as well as faunistic
composition. The number of crustaceans in accumulations might reach tens
of thousands of individuals per cubic meter (Zelickman, 1968a).

However, the general trend in "demographic strategy" in the Arctic
ecosystem is survival through unfavorable conditions and awaiting more
favorable conditions, achieved in many ways. Survival adaptations include,
for example, latent stages of development in animals (N. M. Pertsova,
1974; Prygunkova, 1974; Zelickman, 1972) and the quiescent spores of algae;
the presence of the latter is one factor causing the first climax in the
development of phytoplankton to be observed in the shoals and air holes.

Ecologic differentiation and "waiting strategies" dre also supported
by temperature regulation. During the vegetation season, the temperature
changes over broad limits, making the development of species of various
biogeographic and ecologic complexes possible. The differences in the
peaks in numbers are related to temperature as one of the background
mechanisms regulating the coexistence of the species. The temperature
determines the time of development of the eggs of the Copepoda (N. M.
Pertsova, 1974; McLaren, 1965; Corkett, McLaren, 1970; Corkett, 1972).
The larger the eggs, the longer their development. Considering the
differences in diameter of the eggs of the various species (£. finmarchicus--
145 pm, C. helgolandicus--163 ym; C^. glacial is--178 pm; C. hyperboreus--
190 Mm), it becomes understandable that in zones where the areas of
distribution of these species overlap, the appearance of the young does
not occur at the same time and, consequently, the maximum in numbers is
not reached simultaneously. Furthermore, there is reason to believe
that the acclimation of females which survive the winter to low temperatures
facilitates more rapid development of their eggs (Landry, 1975) and,
consequently, separate utilization of the plant resources in the spring

52

and summer generations of Copepoda. The temperature plasticity of the
eggs of the Copepoda is tremendous (Corkett, McLaren, 1970), which, in
addition to the relative eurybiontity of mature individuals, makes the
disappearance of any species during a single annual cycle in any actual
natural situation impossible.

The regulatory mechanisms guaranteeing the maximum enrichment of the
population during the short period of abundant food also include the
seasonal change in the relationship of the sexes. In the winter, females
predominate among the sexually mature Copepoda, the fraction of males
falling possibly as low as a few thousandths of one percent. The number of
males increases as the mating season approaches, at which time they rapidly
metamorphize from the fourth stage. Another reserve for optimization of
numbers lies in the variability of the number of eggs (McLaren, 1966;
Corkett, McLaren, 1970). It is manifested as seasonal variation of the
number of eggs in the laying and, depending on the number and size of
layings, on the current and previous degree of nutrition of the crustaceans.
A decrease in fertility due to a shortage of food for the Copepoda is thus
reversible. If the deficiency lasts longer, the fertility is decreased
for a long period of time, thus decreasing the nonselective elimination.
Selection by change of the fertility norm touches not only upon the phase
of egg production, but all of ontogenesis. If the population density of
Cyclops is too high, the number of females laying fertilized eggs decreases,
while the period of postembryonal development increases (A. L. Zelickman,
1946; A. L. Zelickman, Heinrich, 1959). The lower the population density
(greater the supply of food), the more closely spaced the emergence of
the nauplii and the higher their survival rate. This is possibly one means
by which the minimal wintering number of Copepoda after a year of low
productivity provides a tremendous population peak during the next spring
cycle (Zelickman, 1960b; Zelickman, Kamshilov, 1960). It cannot be
excluded that when population density is low, exocrine regulation of the
numbers is eliminated.

However, for benthic and interzonal species of Copepoda in the Arctic
community, other adaptations are characteristic, similar to those of the
deep-sea pelagic species, the conditions of existence of which are more
stable (Matthews, 1964; Vinogradov, 1968). It is characteristic for them
that there are no sharp fluctuations in number (Chiridius armatus,
Bradyidius bradyi , Aetideus armatus, Xanthocalanus minor, etc.); the
number of eggs (falling to the bottom") is less than that of the epipelagic
species; the number of layings per year is less; the high amount of vitellus
in the eggs, and, correspondingly, the lecithotrophy of the nauplii; a
decrease in the number of nauplial stages; year-round fertilization of
females; longer duration of the fifth copepodite stage. In the community,
these species "collect the trash," and the period of their relative abun-
dance coincides with the phase of summer decrease of zooplankton in the
upper layer. The temperature regulates the sequence of breeding of the
benthic species and allows them to be spread in terms of times of the
beginning of breeding, providing their progeny with relative regularity of
food supply. In the interzonal dominant species in the high Arctic
waters (C. glacial is, £. hyperboreus, Pareuchaeta spp., Metridia longa),
adaptations are in part similar to those mentioned above; the copepodites

53

live a long time and are capable of fasting for long periods, expending
the high-calorie fat and waxy esthers. An increase in the concentration
of waxy esthers gives the Copepoda neutral buoyancy, compensating for
the loss of energy during the longer active swimming stage. For these
forms, as for deep-sea species, food specialization is characteristically
slight, with a higher share of detritus in the diet and the ability to
change methods of feeding, trapping all potential food when its concentration
is low (Vinogradov, 1968; Mullin, 1963; Mauchline, 1966; Poulet, 1973,
1974). The food spectrum is particularly broad among the eurytopic
species which inhabit the oligotrophic water areas. For example, Mysis
rel icta in the summer feed on detritus, phyto- and zooplankton, while in
the fall, with the beginning of the regular vertical migrations, they
eat only Cladocera; Metridia longa in the summer is primarily a phyto-
planktophage, in the winter feeding on the young of the Copepoda (Lasenby,
Langford, 1973; Haq, 1967). The same features of nonselectivity are
inherent in the epiplankton filter feeders Fritil laria and Oikopleura
(Madin, 1974). The neritic Temora longicornis and Centropages hamatus
can also eat the spores of the Phaeocystis , formerly considered inedible
(Jones, Haq, 1963). Omnivorous tendencies increase in the higher latitudes,
both in predators such as the polychaete Tomopteris septentrional is or
the copepod Pareuchaeta norvegica, the number of which is relatively
stable (Kielhorn, 1952; R. Williams, 1974; Dodson, 1975), and in phytophages.
£. hyperboreus may form a surface and deep-water population in the same
location, the deep-water population being distinguished by a high level
of consumption of microzooplankton. C^. hel golandicus may winter exclusively
by carnivorous eating (Corner et al., 1974), and C. hyperboreus normally
forms eggs on a diet of "meat" (Lee, 1974). The utilization of animal
food by plankters generally increases when food concentrations are low
(Gaudy, 1974).

The time factor is extremely important for the trophies of the Arctic
community. Bacterial mineralization and the decay of dead tissue occur
more slowly in cold water (Harding, 1973), which preserves a larger supply
of food for second-order consumers. The breeding of a number of invertebrate
species in the autumn and winter allows the resources of food to extend
throughout the year. The basis of the biomass of the Arctic community
is created by populations of relatively large, slowly growing organisms with
slow metabolism. This also is facilitated by the great length of life cycles
(1-2. sometimes even 3 years) of Parathemisto, Sagitta , Thysanoessa, etc.
In the boreal waters, these animals have shorter cycles (Bogorov, 1940;
McLaren, 1966, etc.).

2,3. The Seasonal Course of the Process of Production in
the Arctic Community

Let us briefly study the actual picture of production, basically on
the example of the Barents Sea, which is included entirely in the Arctic
basin. Its plankton population is representative for the Arctic community.
It is also important that the Barents Sea is an epicontinental body of
water, while a huge shelf zone is typical for the Arctic.

54

The fluctuations in annual quantity and prevernal reserve of biogens
observed in Arctic waters depend primarily on the intensity of the vital
activity of the plankton. The vernal development of phytoplankton , in any
case in the Barents Sea, is not limited by the reserve of biogens. For
example, in 1958, with the minimal winter reserve of nitrate nitrogen
observed in 1949-1959, a maximal brood of phytoplankton was observed. The
development of phytoplankton begins at minimal temperature and maximum
vertical stability of the euphotic layer. However, by summer the reserve
of biogens is exhausted, and the shortage begins to inhibit the develop-
ment of phytoplankton. Only in regions of abundant bird population, due
to the local enrichment of the littoral waters with biogens, does stable
production of bacterio- and phytoplankton continue throughout the entire
spring and summer (Golovkin, Zelickman, 1965; Zelickman, Golovkin, 1972).

The greatest May peak in development of phytoplankton is that of
Phaeocystis; the April and July peaks formed by the diatoms partially
merge with it; the development of the peridinia is significant in June and
September. The greatest maximum is that of Phaeocystis pouchetii : over
7.8 billion cl/m3 (Roukhiyaynen , 1960), while the scale of the April-May
peak of diatoms is less: over 800 million cl/m^ in the 0-50 m level.
The most productive waters in the spring are the Arctic and mixed waters.
In the summer, the oceanic complex of phytoplankton is replaced by a
neritic complex.

The Calanus and euphausiids, which make up the basis of the winter
biomass of zooplankton, spend October through February at depths of over
150 m. The locus of the winter benthic concentrations of crustaceans and,
correspondingly, the locus of their March-April rise, forces us to think
that the basis of the Barents-Sea superpopulation of these species is the
indigenous population. This is confirmed by morphometric analysis of the
stages of development (Zelickman, 1958, 1968; Zelickman, Golovkin, 1972;
Nesmelova, 1966, 1968). In the Barents Sea, in any case to the east of
the meridian of the Kola (33°30'E), over 70% of the population of plankton
in the Arctic, local and neritic waters, consists of the autochthonous
population.

With respect to time, the first consumers of the phytoplankton are
the nauplii of the barnacles. Reproduction of the barnacles heralds the
beginning of the biologic spring in the Arctic community. The number of
Balanus nauplii appearing on the southeast shore of the Barents Sea,
usually by the 20th of March, increases within a period of a few days
to 40-50'lo3 per cubic meter in the 0-10 m layer. The reproduction of the
Balanus is independent of water temperature. The metamorphosis of the
second nauplial stage into the third, the intensive consumer of phyto-
plankton, coincides with the increase in the number of diatoms. The
barnacles "can wait for" the appearance of suitable conditions for repro-
duction; embryos which have completed their development sometimes wait for
12-18 days in their capsules before the appearance of the nauplii in
plankton. The barnacles precede the spawning of the other massive species,
which allows the larvae to avoid competition during the most vulnerable
stages of ontogenesis.

55

The beginning of breeding of the Calanus and euphausiids and the
rise of the biomass (Fig. 6) coincide with the beginning of blooming of
phytoplankton and is also unrelated to the absolute temperature index
(Zelickman, 1958; Kamshilov, 1952, 1955). Since the spermatophores of
the male of Calanus and euphausiids are formed long before the spring
rising of animals to the surface water, it is possible that spawning
occurs only after a certain period which the mature individuals must
spend in the light. Breeding may occur over a broad temperature range,
approximately identical for all the mass species: for Thysanoessa raschii,
from -1 C to 7-10 C, for T. inermis, from 0-7-10 C, for Calanus, from
-1 to n C. The prespawning concentrations of euphaisiids and Calanus are
formed in the euphotic layer, where their young will later feed. The
oceanic, primarily predatory, forms (Thysanoessa longicaudata, Pareuchaeta
spp. , Metridia spp. ) are less closely related to the phytoplankton;
therefore, their area of breeding is broader and more continuous, their
breeding period more extended. The breeding peaks of the three massive
phytophages are displaced with respect to time; for example, in the
Barents Sea, the Calanus breeds in April, T. inermis in May, T. raschii in
June.

Since the phytoplankton bloom begins in various sections of the water
masses at different times, naturally an alternation develops in the zones
of abundance of the young, then of the mature individuals of the massive
species. Therefore, the relative significance in the increase of the
biomass of the deep water regions and the shallow-water regions changes by
seasons: During the spring-summer season, the biomass of zooplankton is
higher in the shallow water during the fall and winter--in the deep-water
regions. This process of redistribution of living matter is related to
the seasonal ontogenetic migrations and cycles of breeding of the holo-
and meroplankton animals (Fig. 7). The neritic waters (in the comparatively
productive layer) are richer.

The separation of the zones of large numbers of Calanus and young
euphausiids in May-June in waters with abundant phytoplankton bloom can
be explained not only by the competition for food, but also by exocrine
interactions. Generally, direct and indirect trophic and topical inter-
relations of the dominant species of zooplankton with the nannoplanktonic
heterotrophs and with the phytoplankton are very close. Sometimes, these
bonds are broken at the final, trophic level, bypassing the previous
levels. For example, in the neritic communities of colonial birds,
the euphausiids and mysids are eaten in large numbers by thick-billed
guillemots and kittiwakes, the Calanus by the little auk (Zelickman,
1958; Golovkin et al . , 1972). Sometimes, direct expulsion of a species
from its ecologic niche is observed, as occurred in 1956 with Pseudocalanus
elongatus, developing rapidly in Svyatonosskiy Bay of the Barents Sea after
grazing of Calanus finmarchicus there by the Murmanc herring (Zelickman,
1961a).

The summer maximum of zooplankton is created by £. finmarchicus,
Pseudocalanus, Oithona, Oncaea, Fritillaria, Oikopleura, and in August-
September--by abundant small hydromeduses and ctenophores. In the shallow

56

s I la Y M K n I M r ma E i m v viiin i m t nmn i m r wa mi in v mixn
z MI Mil mi MiiNmmiMiiTnminiiiiTTiwins jyb mi mm re mx m
!S5j m^i IS55 ms /^S7 /ffSS

Fig. 6. Perennial dynamics of zooplankton biomass of Barents Sea on the
shore at flurman (section through the Dal'nie Zelentsy traverse). I, water
temperature, 0-50 m; II, mean monthly biomass throughout the entire column
of water, for all plankton (1) and Calanus (2) (Zelickman, Kamshilov, 1960)

Fig. 7. Annual cycle of changes in
biomass of plankton of Barents Sea
by months (ManteyfeT , 1941):
Ordinate, mean plankton biomass for
0-100 m level; 1, littoral waters
from Ringvasse Island to Svyatoy
Nos Cape (1934); 2, southwestern
area of open sea (1939).

/ I JU IF YWMMHIITM

57

neritic zone, the dominant species are recruited from the complex specific
for this zone: Acartia longiremis, A. clausi , A. bifilosa, A. tumida,
Centropages hamatus, £. mcmurrichi , Temora longicornis. In estuaries, to
these forms we must add Limnocalanus grimaldii , Senecella cal anoides ,
Drepanopus bungei , Derjuginia toll i , Heterocope appendiculata , h[. boreal is,
Eurytemora hirundoides, and E. herdmani , the Cladocera and the rotifers.
The biomass of the estuarian complex may reach 30 g/m3, but namely its
productivity fluctuates from season to season by hundreds and thousands of
times.

The most important reason for the seasonal summer-fall decrease in
biomass of zooplankton in the Arctic community is consumption by planktono-
phagous fish, fingerlings of benthic fish, as well as sagittae, medusae
and ctenophores. The elimination of the Copepoda by fish occurs in all
stages of ontogenesis, with not only phytophages, but also predators
involved in the process (Sysoyeva, 1973; Aslanova, 1971). There are a
multitude of invertebrate predators: for example, in the southeastern
portion of the Barents Sea in July and August, the number of ctenophoran
Bolinopsis infundibulum reaches 170 per cubic meter, Pleurobrachia pileus--
30-40 per cubic meter, the medusae Rathkea , Obel ia, Aglantha digitale,
Tiaropsis mul ticirrata--up to 3000 per cubic meter (Zelickman, 1961a, 1966,
1969) . The rate of elimination of the Calanus depends directly on the
population of Bol inopsis : the correlation coefficient between the overall
elimination of Calanus and the occurrence of ctenophores is 0.93±0.06.
In August alone, the Ctenophora may decrease the population of Calanus by
a factor of 5 (Nesmelova, 1968). The peak of the population of medusae
and ctenophores is independent of temperature and is related to the
population of prey, occurring usually 2-4 weeks after the peak of Copepoda
biomass, regardless of the hydrologic specificity of the year, but the
duration of the period of high population of Coelenterata is closely
related to the temperature (Zelickman, 1955; Zelickman, 1972). The
number of invertebrate predators is in turn regulated by a secondary
mechanism--their consumption by more narrowly specialized predators--
other ctenophores and meduses. For example, Beroe cucumis consumes only
Bol inopsis. Tiaropsis multicirrata , when highly concentrated, after
consuming the crustacean zooplankton, begins eating Rathkea octopunctata,
turns to cannibalism, etc. (Zelickman, 1960b, 1965; Zelickman, Kamshilov,
1960; Zelickman, 1972; Conover, Lalli, 1974).

Let us trace this scale of creation of living matter in the Arctic
community, using the Barents Sea as an example. During years with Calanus
domination, the curve of the dynamics of biomass in the plankton has a
single peak (see Fig. 5); as the number of Calanus drops, the curve takes
on more than one peak and the maxima are shifted in time. The annual pro-
duction of Calanus finmarchicus averages 250-300 mg/m3, about 90% of the
annual production occurring between April and early October (Kamishilov,
1958). The higher the biomass of the Calanus , the greater its relative
significance in the plankton. It is logical to presume that with full
realization of its productive potential, Calanus would expel the remaining
zooplankton. Extrapolating the curve of relative significance of Calanus
(Fig. 8) to 99.9%, we obtain the value of the theoretically maximum possible
spring-summer biomass of zooplankton (excluding Protozoa, Medusae, Ctenophora
and other crustaceans) in the upper 50 m layer is about 3 g/m^. This level
of biomass has actually been observed repeatedly. For example, in June-July

58

Fig. 8. Variation between
absolute (abscissa) and relative
(ordinate) values of biomass of
Calanus f inmarchicus s . 1 . in
the plankton of the Barents Sea
(Kamshilov et al . , 1958).

ff 10 so wo /so 200 2S0 JOO JSO '/ffO

mg/ni

of 1975 in the neritic waters of the Barents Sea, the biomass, according
to our data, was about 3 g/m3 in the 0-50 m layer, over 99% of the biomass
being Calanus, with other crustaceans practically absent in the plankton.

The remaining
Calanus in number,
others, damp the po
The flexibil ity of
increases when othe
maximum possible bi
real ization of the
trend in any pelagi
but in the latter i
species. Since abs
occur, it is clear
the pressure of the
even in Calanus, th

members of the community, capable of exceeding the
though not in biomass, such as Oithona , Fritillaria and
ssible excursions of the biomass and of production,
the system, its stability in relationship to deformations,
r species are present, each of which fails to reach its
omass. The "price" of increased stability is incomplete
potential biomass and production, which is a general
c zone community, including the Arctic community,
t is particularly severe for opportunistic, subordinate
olute expulsion of "non-Calanus" zooplankton does not
that certain limiting factors are at work, increasing
environment on the dominant species. Consequently,
e reproductive potential is not fully realized.

In the Arctic community, as in general in communities with nonrigid
hierarchic structure, the species following the dominant species in rank,
in case of a decrease in the number of the latter, takes its place. In
hydrologically unfavorable years, the total biomass remains at the median
level, but the relationship of the dominant groups, primarily in the
neritic zone, changes: In the White Sea, for example, the cladoceran
take first place in terms of biomass rather than the copepods; in the
estuarine Arctic plankton, the most numerous is at times Limnocalanus at
times Drepanopus , at times Senecel la or the Cladocera.

The maxima in the Arctic plankton population curve may be numerous,
up to 7-8 in neritic waters (Fig. 9), with the curve of the annual course
of biomass having two, less frequently, three peaks. The course of the
curves of the dynamics of the populations of primarily carnivorous plankters
is more complex than that of primarily phytophagous plankters (Fig. 9A).
The smaller peaks of individual groups late in the year may merge (Fig. 98).
Variations of this type have been traced by many authors for the Barents
Sea (Manteyfel ' , 1939, 1941; Zelickman, Kamshilov, 1960), the Norwegian Sea

59

Fig. 9. Annual cycle of changes in
population of zooplankton in 1955-
1956 at Igloolik (Fury and Hekla
Strait, Canadian Arctic) (Grainger,
1959). Ordinate--number of
specimens in the 0-50 m layer,
abscissa--months; A, mainly
predatory; B, mainly phytoplankton;
1, Copepoda, 2, all zooplankton;
3. Copepoda nauplii; 4, Cirripedia
nauplii; 5, Polychaeta larvae;
1, 3--0.24 mm mesh size; 2, 4,
5--0.57 mm mesh size.

YM n:

JOOOr

zooo

woo

(Wiborg, 1954), Greenland Sea (Kielhorn, 1952; Digby, 1953; Grainger,
1959; Gruzov, 1963; Pavshtiks, 1972) and the White Sea (Konoplya, Kokin,
1973; Kolosova, 1975). The further north the zone in question, the fewer
the number of peaks on the curve, with the meroplanktonic elements of
the community disappearing first. In the high Arctic subarea, the general-
ized characteristics of seasonal development of zooplankton do not differ
in principle from those in the low-Arctic subarea (Digby, 1953; Hughes,
1968; Pavshtiks, 1972). Only the absolute biomass and time parameters vary,
while the number of peaks decreases.

In the Arctic community,
on the latitude. The further
the spring-summer and summer-
the Arctic, the spring proces
earlier in the neritic water,
seasonal changes in the zoopl
also occur in the summer, but
and below 250 m remains pract
Cubic meter for each species
1966; Hughes, 1968; Hopkins,
particularly in the lower hor
seasonal increase in the infl

the length of the biologic seasons depends

north, the more the times of appearance of
fall faunistic complexes come together. In
ses of blooming of the water always begin

over shallows and along the ice fields. The
ankton population beneath the continuous ice

the number of animals increases but little,
ically unchanged, less than 1 specimen per
(Vircetis, 1957; Pavshtiks, 1971a, b; Harding,
1969). However, the species variety increases,
izons of the Central Polar Basin, due to the
ux of Atlantic water with its rich fauna. "!"he

60

predatory and partially predatory forms--Metridia Tonga, Calanus glacialis,
C^. hyperboreus , Pareuchaeta spp., large sagittae, mature medusae Aglantha
and Cyanea , Ctenophora, Amphipoda--are present in small quantities through-
out the year. The growth of biomass in the 0-50 m layer in the high-Arctic
zone at first also occurs due to rising of the animals from the depths,
then due to their breeding and growth. The number of small predators--
Oithona si mil is and Oncaea boreal is--increases in the summer. The
Calanus and Githona may represent 95-99% of the total number of plankters.
The number of Calanus increases beginning in mid-May, decreasing in
September, after which the number of small Copepoda increases. The popu-
lation peak of the relatively larger meduses and ctenophores occurs in
April-May, of the smaller forms--in July-August, synchronously with the
Appendicularia. The fraction of predators in high-Arctic waters is high:
The number of mature large predators is only one or two orders of magni-
tude less than the number of Calanuses. The total biomass, from 20 mg/m^
in late March, increases to 250 in the second half of April -May and 400 in
August, dropping to 200 in late September and then rapidly decreasing to
the winter values (data for the northern area of the greenland Sea). The
winter stock inhabits the lower layer, dropping to depths of over 1000 m.
The various species descend at different times. The Metridia, Microcalanus,
Pareuchaeta, and Spiratella breed in the winter. In zones with intensive
horizontal movement of masses of water (e.g., Scoresby Sound), the
indigenous plankton reaches only 13% of its summer population maximum
(Digby, 1953). In the epicontinental seas and on the shelf, the vernal
maximum consists more than 70-80% of indigenous populations.

2.4. Perennial Changes in the Biomass of Zooplankton of the
Arctic Pelagic Zone ~~~

The productivity of the Arctic community is a resultant quantity from
a complex net of biotic relationships, functioning against the background
of cyclic changes in abiotic factors. Both the deep-sea and the shelf
and neritic water areas represent quasi-stable fields of production with
definite gradients in space and time, preserved from year to year and
generally independent in the temperature aspect. Thus, in the Norwegian
Sea in 1959-1963, the mean annual values of biomass and production
of zooplankton for the sea as a whole differed from year to year by a
factor of not over 2 (Timokhina, 1968, 1972). In the Barents Sea in
1934-1939, the mean annual indicators were approximately the same
(Yashnov, 1940). The production is invariably highest in the Arctic and
shore waters (averaging 55 t/km^) and lowest in the warm Atlantic waters
(averaging 9 t/km^). The maxima of production and biomass of the dominant
species occur in various water masses, or diverged vertically or horizontally
through a single mass of water (Zelickman, Kamshilov, 1960; Zelickman,
Golovkin, 1972; Timokhina, 1968).

An analysis of a representative series of 22 years of almost monthly
plankton samples collected by a Longhurst-Hardy automatic plankton
sampler at a depth of 10 m in the north Atlantic showed no clear connection
between climatic changes and seasonal fluctuations in the abundance of
zooplankton. It showed only that various species or groups of species have

61

varying tendencies of changes in their number within and between years
(Colebrook, 1972a, b). The greatest limits of variability in numbers are
seen as we compare different species; the differences are significantly
less when we compare plankton as a whole for different months, least of
all when we compare different years (Colebrook, 1972a, b). The number of
Copepoda before the beginning of the spring development differed in
different years by a factor of less than 2, regardless of the preceding
and subsequent peaks. The times of appearance of the maxima in the numbers
of Copepoda, the duration of the peaks and the scale of the second,
usually smaller, maximum were more variable.

Of particular interest for a general description of the ecosystem
is the slight variability of annual production indicators (Table 2).

This variability from year to year is somewhat greater in the shallow
southeastern area of the Barents Sea (Table 3), where the significance of
invertebrate predators is somewhat greater, decreasing the summer-autumn
biomass to 1/4-1/5 of the previous level (Nesmelova, 1968; Zelickman,
1961c).

The relative constancy in the values of production is maintained by
various mechanisms which standardize the population, acting primarily on
the early stages of ontogenesis. For example, the relative constancy of
the number of Calanus nauplii indicates constancy of the number of breeding
females, capable of maintaining the initial numerical level of nauplii.
The number of Calanus nauplii in a cross section through the Kola meridian
in May (Degtyareva, 1972) is given below:

Year

1959

1960

1961

1962

1963

1965

1969

Specimens/

m3

1103

1011

1019

1130

297

1101

1651

In 40 years of studies of plankton of the Barents Sea, samples were
taken during periods of cooling and warming of the Arctic, covering various
stages of activity of the fishing industry, changing the plankton consumers.
Therefore, it is useful to look at a few more figures. In the southwestern
Barents Sea during the warming trend (1929-1937), the biomass of zooplankton
in the 0-50 m layer averaged 5-15 mg/m3 in December-March, 100-200 mg/m3 in
April, 500-900 mg/m^ in June, with the individual maximums rising to 5000 mg/m^
(Manteyfer , 1939, 1941; Yashnov, 1939, 1940). It remained approximately
the same in 1954-1969, which saw both very warm and \jery cold years. In
the southeastern portion of the Norwegian Sea, the biomass was the same
during warm (1927-1939) and cold (1949-1951) years (Wiborg, 1954). Along
the shores of Spitsbergen in 1959-1966, the seasonal and annual total
volume of plankton in the 0-25 m layer varied by approximately an order of

62

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63

Table 3. Mean annual and mean maximal values of zooplankton biomass
(mg/m3) through entire thickness of water in the southeastern part of the
Barents Sea (Zelickman, Kamshilov, 1960, modified).

Biomass 1951 1952 1953 1954 1955 1956 1957 1958

Mean annual 100 23 45 129 71 67 60 48
Mean maximal - - 287 300 291 93 45 337

magnitude (Lie, 1968b), while fluctuations in the 100-600 m layer did not
exceed 0.05 ml/m^ (Lie, 1968b). The number of mature euphausiids of
Thysanoessa inermis and T. raschii (by trawl net collections) in the
Barents Sea in 1954-19752 varied by a factor of 3-4 (Drobysheva, Soboleva,
1976). Five-year annual collections in Chupa Bay (White Sea) showed
that the zooplankton population in the 0-60 m layer was approximately 10
times as numerous in July as in January, the biomass being about 4-5
times greater (Prygunkova, 1974).

The data presented above indicate that zooplankton of the Arctic
community, in spite of significant perturbations in climate and the
hundred-year pressure of anthropogenic factors, has retained a rather
stable mean level of production, indicating clear homeostasis of the
System. Consequently, Arctic plankton can withstand significant stress,
while retaining its stability and integrity. The matter is quite different
with the nekton. As a result of fishing, the economically valuable
species which previously predominated have greatly decreased in number,
their niches being immediately occupied by other plankton consumers,
less valuable from the human point of view. Thus, the herring have been
replaced by poutassou, the feeding areas of the cod, pollock and haddock
have been partially occupied by the Arctic cod and capelin (Sonina, 1969.
1973; Ponomarenko, 1968). The zooplankton population can drop irreversibly
only in response to very basic changes in the substratum (e.g., an increase
in pollution) and (or) human interference in the interrelationships of the
basic units of the ecosystem.

64

3. Communities of the Temperate Waters of the Northern Hemisphere
Is. A. Mileikovsky, L. A. Ponomareva, T. N. Semenova)

3.1 . Some Biological Peculiarities of Planktonic Communities in
the Co1d-Temperate Regions of the Northern Hemisphere

V. G. Bogorov (1941, 1974) worked out a scheme of biologic seasonal
cycle in the plankton of the temperate waters of the northern hemisphere,
describing its annual cycle as bicyclic with four phenologic (biologic)
seasons. During biologic winter, the annual minimum of plankton occurs
with predominance of zooplankton over phytoplankton. The biologic spring
is the time of the annual maximum of plankton biomass, with significant
predominance of phytoplankton. In the summer, the zooplankton reaches its
maximum, while the total biomass of plankton decreases, and the biomass of
phytoplankton becomes equal to or less than the biomass of zooplankton. At
the end of the summer and in the fall, a second, smaller maximum of phyto-
plankton develops, and at the end of the fall it begins to decrease, leading
to the winter minimum. During the course of the annual cycle, the develop-
ment of phytoplankton precedes that of zooplankton, the difference
between the maxima and minima of phytoplankton being greater than is the
case for the zooplankton.

The scheme of V. G. Bogorov, however, was constructed practically
completely on materials observed in the North Atlantic. A. K. Heinrich
(1961a) developed the scheme further and made it much more specific by
considering the extensive material available concerning the North Pacific.
She showed that the annual cycles of the various species of zooplankton are
too different to allow any biologic season in the plankton to be described only
by specific age composition of the whole zooplankton. Similarly, we cannot
find identical characteristics of analogous seasons in terms of the relation-
ship between the quantities of phytoplankton and zooplankton for all regions
in the temperate latitudes. Therefore, the characteristics suggested by
V. G. Bogorov (1941) are not applicable to the temperate latitudes as a
whole.

In the opinion of A. K. Geinrich, as we attempt to differentiate
the biologic seasons in the marine plankton, we must base our discussion
on different characteristics from those used by V. G. Bogorov. The annual
cycle can be divided into natural segments, each of which is characterized
by a definite group of seasonal species present in the plankton only during
this time segment, and a definite stage in the life cycle (annual maximum)
of year-round species. However, due to the gradual nature of replacement of
one group of species by another, any seasonal boundaries we select are
arbitrary to some extent. The clearest boundary between seasons in the
cold-temperate regions is the boundary between winter and spring, which
marks the beginning of the vegetation of the phytoplankton.

In the zooplankton of the cold-temperate regions of the northern
hemisphere, a very important role is played by a few common genera of

65

phytophagous copepods; Calanus , Pseudocalanus, Metridia, etc. Among the
holoplanktonic phytophagous forms, three types of life cycles can be
distinguished (Heinrich, 1961a). The first type includes species in which
breeding of the first generation is related to the spring development of
phytoplankton and cannot begin any earlier. This type of life cycle is
exhibited by Calanus finmarchicus , dominant in planktonic communities of
the temperate waters of the North Atlantic (Marshall, Orr, 1955; Bogorov,
1941), as a result of which the annual maximum zooplankton biomass follows
the spring pulse of phytoplankton. A modification of this type is the life
cycle in which breeding and growth can occur only when phytoplankton is
sufficiently abundant; the transition from the last copepodite stage to
the adult occurring at the beginning of the period of phytoplankton vegeta-
tion. In regions of domination of these species (e.g., Eucalanus bungii in the
Bering Sea and northwestern Pacific), the annual maximum of zooplankton
biomass is seen in the spring (Heinrich, 1957, 1961a).

The second type of life cycle is exhibited by forms, the breeding of
which is independent of the quantity of phytoplankton and may occur either
in spring, or in other seasons: Calanus cristatus and C^. plumchrus in the
North Pacific, Metridia longa and C^. hyperboreus in the North Atlantic.
Species with life cycles of the first and second types usually have 1-3
generations per year in the cold-temperate regions.

The third type of life cycle is that of species which can multiply
throughout the year, but do so most rapidly during the period of vegetation
of the phytoplankton. Most of the smaller forms of copepods fall into
this group, and have several generations per year.

A. K. Heinrich (1961a) also reports that the presence in the plankton
of the cold-temperate regions of certain neritic species of Cladocera and
Copepoda is always a characteristic of the summer and early fall.

The breeding of predaceous copepods, for example, Pareuchaeta spp., in
the opinion of A. K. Heinrich, is independent of the phytoplankton and is
not limited by the presence of animal food, which is always sufficient;
these species breed throughout the year. However, the abundance of phyto-
plankton does determine the success of the breeding of phytophagous
zooplankton and, therefore, the food base available for the predators. Data
on common pelagic polychaetes, the pteropod mollusk Clione limacina and
chaetognaths (Kaufman, 1967; Mileikovsky, 1962, 1969", 1970; Dunbar, 1962)
indicate that seasonal breeding is a common phenomenon among predatory
holoplankters of the cold-temperate communities.

Among the widespread, common species, the peculiarities of the life
cycle change with latitude and may differ in the southern and northern
portions of their ranges. The number of generat"'ons during one reproductive
season, in particular, differs with latitude: The further north, the fewer
the number of generations.

In the cold-temperate zone, the nature of the sequence in maxima of
biomass of phytoplankton and zooplankton is determined by the type of life

66

cycle of the dominant species. A bicyclic annual course of development of
plankton is characteristic for the entire zone; the specifics of develop-
ment of plankton is characteristic for the entire zone; the specifics of
development of phytoplankton and zooplankton in the waters of the North
Atlantic and North Pacific differ somewhat. In the North Atlantic, with
domination of Calanus finmarchicus , the annual maximum of zooplankton
biomass follows the spring annual maximum of phytoplankton with some delay,
while the autumn, smaller, maximum of phytoplankton is followed by a small
autumn rise in the biomass of zooplankton. Significant consumption of
phytoplankton by zooplankton begins a few weeks after the beginning of
development of the phytoplankton and coincides with the appearance of the
II and III copepodites--soon after the massive spawn of C^. finmarchicus
having survived the winter (Gushing, 1975). It is characteristic of the
temperate waters of the North Atlantic on the whole that the spring peak of
development of phytoplankton is greater than the fall peak, and that the
amplitude of the fall peak varies from yesr to year.

In the northwest Pacific and the Bering Sea, where the common species
in zooplankton are C^. cristatus, C_. pacificus, C. plumchrus and Eucalanus
bungii (the first three species are Pacific analogs of the North Atlantic),
the bicyclic development of phytoplankton, "normal" for temperate waters,
is observed only in the neritic regions. In the oceanic regions, only
a fall maximum of biomass of phytoplankton is observed, while the annual
maximum of zooplankton biomass occurs in the spring and summer, when the
phytoplankton is rather abundant (Heinrich, 1951a).

The duration of the production cycle of plankton varies from one
month to one year, averaging three months for phytoplankton and six to
seven months for zooplankton. The fluctuations in production cycles of
plankton from year to year reach two or three orders of magnitude as to
population of algae and one or two orders for the biomass of animals. The
differences between the mean values for different years in the same regions
are less than between different seasons in the same year (Gushing, 1975).

The mean value of annual production of planktonic phytophages in
productive regions, where they represent most of the biomass in the 0-500 m
layer, has been estimated as 200-300 mg/m3 (Greze, 1973a).

We must note one important specific feature of the cold-temperate
regions of the northern hemisphere which is becoming more significant with
each passing year: the continuous increase in the effects of anthropogenic
factors on the plankton communities, particularly water pollution. These
waters wash the shores of the most industrially developed countries in the
world, and their coast sections are the most polluted portions of the world
ocean. Pollution has a significant and ever increasing effect on the biology
of plankton communities in most regions in this zone. To illustrate this
statement, it is sufficient to present two examples. In the northwestern
Atlantic, over the edge of the continental shelf and somewhat further out
to sea, lumps of tar floating on the surface now equal more than 20% of
the wet weight of all neuston (Morris, 1971). Between Hawaii and Japan for
mile after mile, one observes films of copepod remains, which have died as

67

a result of pollution of the water along the coast of Japan (Lee, Williams,
1974).

3.2 Planktonic Communities of the Boreal Atlantic

The pelagic communities of the Boreal waters of the North Atlantic are
related in their distribution to the superficial subarctic water mass
(Mamayev, 1960; Jaschnov, 1961; Grainger, 1964; C. W. Beklemishev, 1969).
Within this area, a number of large regions can be distinguished, differing
in their latitudinal position, the presence of a more or less closed system
of water circulation and, as a result, the structure of the planktonic
communities and the dynamics of seasonal processes. These relatively
independent regions include the Norwegian Sea with its circulation formed
by the system of Norwegian and East Iceland Currents; the Labrador Basin,
with the circulation of the West Greenland and Labrador Currents; the open
portion of the North Atlantic, to the north of the main flow of the North
Atlantic Current, with its less clear circulation formed by the peripheral
streams of the North Atlantic Current, the Irminger Current, and the eastern
branch of the Labrador Current.* One general regularity in the hydrologic
mode of these regions is the predominance of cyclonic water circulation.
Cyclonic flow also predominates in the movement of air masses here (Bulatov,
1971). This creates favorable conditions for upwelling of deep water, rich
in biogenic elements, and, therefore, for abundant development of plankton
and the formation of concentrations of commercial fish.

The taxonomic composition of the zooplankton of the Norwegian Sea, the
Labrador Basin and adjacent waters in the open North Atlantic is similar
in its main features, the difference resulting from the intrusion of
warm-water elements with the waters of the North Atlantic Current and
cold-water forms with the Arctic waters.

The predominant role is that of the copepods, particularly the most
abundant species, Calanus finmarchicus s.l. During some seasons in the
Norwegian Sea and the Labrador Basin, these crustaceans may represent more
than 90% of the biomass of all zooplankton. The growth and development of
C_. finmarchicus from egg to the older copepodite stages produces the
summer increase in total biomass and the maximum concentrations of plankton.
The population of C^. finmarchicus in the 0-200 m layer decreases in the
fall, as a result of intensive predation by planktophagous fish, and also
due to the gradual descent of the fourth and fifth copepodite stages into the
depths, where they spend the winter.

Due to the existence of more or less closed systems of water circulation,
the Labrador Basin and Norwegian Sea support large, independent populations
of C. finmarchicus s.l. It is more difficult to determine the nature of
the population of the species inhabiting the open waters of the North
Atlantic. Doubtless, it is supplemented by constant intrusion of a portion

*In accordance with the purpose of the present monograph, primary
attention will be given to oceanic plankton communities, while the regions
of the North Sea, the Grand Banks and the Gulf of Maine will not be analyzed,

68

of the population from the Labrador Basin, which communicates broadly with
the adjacent waters of the open North Atlantic. The North Atlantic Current
may carry these crustaceans to the northeast and even through the Faeroe-
Shetland Channel into the southern area of the Norwegian Sea. On the other
hand, a portion of the population of C. finmarchicus from the Norwegian Sea
is carried along with the East Iceland Current into the open North Atlantic
and subsequently may be carried to the south and west. Thus, these two,
large, independent populations of this species may be interconnected by
means of a third population, less numerous and more or less dependent on
the first two. We should keep in mind the fact that, in spite of the
predominance of transport water in the northeastern direction, the open
portion of the North Atlantic which we are considering does have its own
cyclonic system of circulation of water masses, though it is highly complex
and not clearly expressed. Therefore, the population of C^. finmarchicus
which inhabits this area cannot be considered totally dependent. In part,
it may be drawn into the circulation or may be delayed for an indefinite
period in any portion of the circulation due to eddies in the current,
e.g., in the region of the Irminger Sea.

In zones of mixing of subarctic waters with the waters of the Polar
Basin (Davis Strait, northeast of the Norwegian Sea), C^. finmarchicus s. str.
is found together with its close relative C. gl acial is and with £. hyperboreus-
species which occupy the Arctic area, but penetrate with streams of cold
water into the temperate latitudes (Jaschnov, 1963, 1970). To the south of
the Faeroe-Shetland Channel, in the northeastern Atlantic, C. finmarchicus
s. str. is found together with another relative species--£. hel golandicus
(Marshall, Orr, 1955; Jaschnov, 1961). This species, a part of the
Lusitanian faunistic complex, is carried into the Norwegian Sea and the
nrothwest Atlantic only sporadically. In contrast to the species we have
mentioned, C. finmarchicus s. str. is a true boreal species, endemic for the
temperate regions of the Atlantic Ocean (Jaschnov, 1961, 1970).

Among other species of copepod filter feeders, in the boreal waters
of the North Atlantic, Pseudocalanus elongatus and £. minutus are present
in great quantities. The former (smaller) species is particularly numerous
in shallow waters over the shelf; the latter is found primarily in the
oceanic zone and plays a significant role in the pelagic communities of
the Labrador Basin (Pavshtiks, 1969; Kielhorn, 1952) and the Norwegian Sea
(Pavshtiks, Timokhina, 1972; Wiborg, 1954). These species are morphologically
difficult to distinguish, and their biology has not been sufficiently
studied. Their reproductive season is quite extended: practically all
summer, in addition to the mature individuals of both species, the plankton
contains their nauplial and early copepodite stages. Obviously, during
the year £. elongatus and £. minutus breed several times, but different
breeding periods are difficult to distinguish. The greatest number of
Pseudocalanus in different years in the North Atlantic may occur in
different months during the spring, summer or fall; in the Norwegian Sea
it is most frequently observed in the summer or fall (Gruzov, 1963; Wiborg,
1954, 1955). In contrast to the Norwegian and Labrador Seas, in the open
North Atlantic, Pseudocalanus spp. are not a significant fraction of the
plankton, being usually replaced by more thermophilic and oceanic species

69

of the genera Paracalanus, Ctenocalanus and Clausocalanus , which, in
spite of their small size, sometimes represent a significant fraction of
the zooplankton biomass (Kanaeva, 1962). In the Labrador Basin and the
Norwegian Sea, Paracalanus and Clausocalanus are not numerous.

Yet another small species of copepod reaches significant numbers in
the boreal waters of the North Atl antic- -Mi crocal anus pusillus . Information
on its life cycle and the nature of its feeding is almost totally
absent from the literature. It is assumed (S. M. Marshall, 1949) that
M. pusillus feeds on flagellatae.

Among the copepods with mixed diet, Metridia lucens is most important
in the North Atlantic, being ubiquitous, although it is most frequently
encountered in the southern portion of the boreal area: in the region
of the Flemish Cape Bank, in the open waters of the boreal Atlantic, in
the southern part of the Norwegian Sea (Kanaeva, 1963; Semenova, 1964;
Timokhina, 1968). However, this species never represents a great biomass
and, in this respect, is quite different from the similar Far Eastern
species M. pacifica , which may form significant concentrations. The
breeding season of M. lucens in the North Atlantic is extended: The
nauplii and juvenile forms are encountered throughout the year, though
most numerous in spring and fall; the species achieves its highest
number in late summer (Gruzov, 1963). Another species of the genus--M.
longa--is an Arctic one, although it can penetrate far into the temperate
regions with cold currents, where it usually is seen together with C.
jlacial is and C^. hyperboreus. In mixed waters in the northern part of
the boreal area, M. Tonga is quite common and, due to its large dimensions,
may represent a significant fraction of the zooplankton biomass (Pavshtiks,
1964; Timokhina, 1968). In the open waters of the boreal Atlantic, in the
southern portion of the Labrador and Norwegian Seas, Pleuromamma robusta
is rather common, and sometimes one also sees P^. abdominal is, P. xiphias,
P. boreal is and £. gracil is, which are common in the subtropics and reach
the southern portion of the boreal area with the North Atlantic Current.

Among the other euryphagous copepods for the boreal Atlantic, we should
note Scolecithricel la minor. The small euryphagous calanoids form a
unique complex: Acartia clausi , Centropages hamatus, £. typicus, Temo ra
Ipngicornis . They are found primarily in the neritic zone, but extend
widely into the central waters of the Labrador Basin and the Norwegian
Sea as well. Their numbers may be relatively high, particularly in late
summer-early fall, but due to their small size they usually are not
significant in the total mass of plankton. Their breeding period is
extended, occurring primarily in the spring and summer, they are rare in
the open waters of the North Atlantic,

There are not many abundant species of predaceous copepods in the
boreal area of the Atlantic. The most important one is Pareuchaeta
norvegica, which, due to its large size and ability to form concentrations,
plays a significant role in the pelagic community and represents an important
component in the nutrition of the planktophagous fish. Furthermore, P.
norvegica, extending over a broad range of depths, is frequently eaten by

70

commercial fish, such as young redfish (Konchina, 1968). The same is true
of Heterorhabdus norvegicus, although this copepod is not numerous and its
role in the plankton is much more modest. Not being related to the period
of vegetation of the phytoplankton, the predaceous copepods breed year-
round and may be greatest in number when the phytophages are at their
period of minimal development, for example, during the fall and winter
season, as is observed for P_. norvegica in the Norwegian Sea.

The Cyclopoida are represented in the plankton of the boreal Atlantic
primarily by species of the families Oithonidae and Oncaeidae, which
include some abundant species: the cosmopolitan Oithona similis, the
Arctic-boreal Oncaea boreal is and the boreal Oithona atlantica and Oncaea
coni fera . The population of 0. simil is is relatively large throughout the
year, forming a sort of background against which the peaks of development
of the other plentiful species of copepods appear in sequence. In winter,
when the number of other copepods decreases, 0^. simil is moves to first
place, composing 60-70% of the total number of zooplankton. In contrast to
it, 0_. boreal is has its peak in number in late spring and early summer.
During this period in the Norwegian Sea it may amount to 10-30% of the
total zooplankton population; this is significant, recalling that in this
season the total number of planktonic animals is generally quite high
(Gruzov, 1963). Approximately the same relationships are characteristic
for these species in the Labrador Basin (Pavshtiks, 1966). In the open
waters of the boreal Atlantic, the significance of 0^. atlantica and 0.
coni fera, which are not numerous in the northern portion of the boreal
aresy increases.

The next group after the copepods, quite important in the creation of
high biomasses of zooplankton in the boreal Atlantic, is the Euphausiacea .
Of these, most numerous are Thysanoessa longicaudata and Meganyctiphanes
norvegica--borea1 oceanic species. Th. longicaudata forms accumulations
primarily in the surface zone. M. norvegica is less numerous and is
encountered primarily at depths of 200-500 m, though it frequently rises to
the surface. Both species are euryphagous, feeding primarily on detritus
and phytoplankton (Mauchline, Fisher, 1969); therefore, their life cycle
is related to the period of vegetation of the planktonic algae. The
reproductive season of Th. longicaudata in the Labrador Basin extends from
May through September, with the greatest number observed in July-
August, while in winter only mature individuals are seen (Kielhorn, 1952).
In waters of Atlantic origin in the Norwegian Sea, the greatest biomass
of euphausiids is seen in May and June (Gruzov, 1963; Timokhina, 1968).

Among the boreal hyperiid amphipods, Parathemisto abyssorum is most
important in the North Atlantic. Juvenile Parathemisto are seen in the
largest numbers in spring and early summer.

The groups of planktonic crustaceans which we have considered: copepods,
euphausiids and hyperiids, are determinant in the formation of the food
Supply for commercial planktophagous fish. In addition to them, the active
planktonic predators are quite significant in the Atlantic boreal communities:

71

the Chaetognatha, Hydromedusae and Ctenophora. Though they do not make a
significant fraction of the diet of the animals at higher trophic levels
they, nevertheless, may influence their distribution, by consuming the
planktonic crustaceans to a significant extent and greatly reducing their
biomass. Of the chaetognaths , the most numerous are Sagitta elegans and
Eukrohnia hamata, regularly encountered in the plankton throughout the
year. Their greatest numbers are observed in the Norwegian Sea in late
spring and early summer (Gruzov, 1963), when they may represent up to 20%
of the plankton biomass. In the Labrador Basin, they are also present in
the plankton throughout the year: S^. elegans is encountered primarily
in the surface zone near the continental slope, while E. hamata is more
oceanically distributed and is found over a greater range of depths
(Kielhorn, 1952). The chaetognaths are not as important in the boreal
communities of the Atlantic as they are in certain tropical communities of
the world ocean, either in terms of number or in terms of biomass.

The hydromedusa Aglantha digitale, widespread in the Arctic and
temperate regions, may form great concentrations in the temperate waters
of the iJorth Atlantic. In the central regions of the Norwegian Sea, it
develops in large numbers, regardless of the hydrologic conditions of the
year, approximately one month after C. finmarchicus s.l. reaches its
maximum population, usually in July. At this point there is a sudden drop
in the population and biomass of Calanus (Timokhina, 1968). A negative
correlation has been found between the population of A. digitale and C^.
finmarchicus s.l . (Gruzov, 1963; Pavshtiks, 1964).

Seasonal changes in the plankton communities of the boreal Atlantic
have been studied in some detail for the Norwegian Sea, less for the
Labrador Basin, and still less for the open waters of the boreal Atlantic.
The season of biologic spring, characterized by the maximum development
of phytoplankton and the beginning of breeding of C^. finmarchicus s.l.,
the Euphausiacea and certain others, begins earliest in the southern regions
of the boreal area, then gradually extends northward, being delayed in the
northern boreal waters by 2-3 months in comparison to the southern boreal
waters. Figure 10, based on the data of Pavshtiks (1966, 1969), Timokhina
(1962), Semenova (1964), Colebrook and Robinson (1965), shows the times
when biologic spring begins in the various regions of the boreal Atlantic.
Spring starts in the coastal waters of the southern boreal zone (February-
March), then encompasses the regions of the North Sea and the oceanic area
of the Atlantic south of 59°N (March-April). In May and June, biologic
spring extends to the central regions of the Labrador Basin and the
Norwegian Sea and, finally, in June-July, biologic spring extends into the
northern boreal regions of the Davis Strait and the northeastern area of
the Norwegian Sea. The maximum development of phytoplankton is followed by
a gradual increase in the biomass of phytophages. In the southern boreal
regions, the times of the maxima are closer together (Fig. 11). In the
Central areas of the Norwegian and Labrador Seas, the maximum biomass of
zooplankton is delayed by approximately one month relative to the peak of
production of phytoplankton: In the central waters of the Norwegian Sea,
the maximum biomass of Calanus usually occurs in June.

72

Fig. lu. Times (months) of onset of biologic spring in arious regions of
the boreal Atlantic (Pavshtiks, 1968; Pavshtiks, Timokhina, 1972; Colebrook,
Robinson, 1965).

Fig. 11. Times of maximum development t
phytoplankton and of the biomass of
copepods in the southern boreal waters
of the open Atlantic (Colebrook, Robinson.
1965). 1, Phytoplankton number;
2, Copepod number (relative values).

IMF HI H U

c s n win

73

During the year, the maxima of population of the individual species
follow one another in sequence. This phenomenon has been analyzed in
detail by L. N. Gruzov (1963) for various regions of the Norwegian Sea.
The relative significance of individual species in the community also
changes significantly from season to season. The differences from year
to year in the development of plankton have been most thoroughly studied
for the Norwegian Sea. Although in the open regions of the North Atlantic,
regular multiannual collections of plankton have also been made using an
automatic continuous plankton recorder, these data are difficult to compare
with the materials obtained using plankton nets. The differences from
year to year in the development of the plankton of the Labrador Basin have
not been studied, but it has been demonstrated for the Norwegian Sea
(Pavshtiks, Timokhina, 1972) that the beginning of biologic spring and
the duration of the seasons in the plankton depend on many abiotic factors,
particularly the number of sunny, storm-free days in March and April,
the intensity of the influx of warm water with the Norwegian Current, the
degree of summer heating of the water, etc. Storms and overall cloud cover
during the spring months delay the development of phytoplankton and the
subsequent mass breeding of the crustaceans. During relatively cold years
(1958, 1962, 1965, 1966), a delay and an extension in the time of biologic
spring has been observed in comparison to moderately warm or warm (1960)
years. Depending on abiotic factors, the interrelationships of species
within a community change from year to year. For example, the largest number
of the hydromedusa A. digitale occurs during cold years (1962-1963), the
maximum biomass--during warm years (1960-1961) (Timokhina, 1968). Apparently,
this is a result of the more rapid growth of medusae during warm years.
Since the number of medusae influences the number of planktonic crustaceans,
during different years the production of different links in the plankton
community may differ significantly (Table 4).

Table 4. Production of main forms of zooplankton over entire Norwegian Sea
area, occupied by Atlantic waters, in 1959-1963 (in millions of tons)
(Timokhina, 1968).

Species

1959

1960

1961

1962

1963

Calanus finmarchicus

7.33

6.46

4.13

8.51

4.88

Calanus hyperboreus

2.24

0.58

1.01

3.07

0.24

Metridia longa

1.64

1.00

0.57

2.59

0.94

Metridia lucens

0.36

0.007

0.20

--

0.44

Pseudocalanus elongatus

0.64

0.39

0.21

0.26

0.44

Githona similis

0.35

0.007

0.007

0.17

0.17

Oithona atlantica

0.16

0.03

0.05

0.25

0.32

Oncaea boreal is

0.13

--

0.007

0.15

0.29

Aglantha digitale

8.40

20.89

21.51

49.90

20.10

Chaetognatha

6.40

3.69

1.08

1.84

0.84

74

According to the classification of V. G. Bogorov (1967), the boreal
area of the North Atlantic must be considered a highly productive
region of the world ocean. During the spring and summer, the biomass of
zooplankton in many regions of the Labrador Basin and the Norwegian Sea
reaches 500 mg/m3, in many cases exceeding 1000 mg/m3 (Pavshtiks, 1966;
Timokhina, 1968; Vladimirskaya, 1972). The biomass of all seston may be
2-3 times greater. In the fall and winter season, the biomass is rela-
tively low, rarely exceeding 50 mg/m3.

An attempt to calculate the production of main components of plankton
communities in various water masses of the Norwegian Sea was made by
A. F. Timokhina (1968). Based on the materials of multiannual seasonal
plankton surveys, the annual production of the most numerous representatives
of the zooplankton in the Atlantic and mixed waters of the Norwegian Sea
has been calculated, and is presented in Table 5. These quantities should
be considered as minimal, since they do not include the production of the
euphausiids or hyperiids, due to the insufficient degree of study of the
annual dynamics of the number of these groups; the production of medusae,
on the other hand, may be exaggerated, since the calculations were based
on wet weight. The maximum annual production of phytophagous zooplankton
in the Atlantic waters of the Norwegian Sea is 22 g/m^, in the mixed waters--
73 g/m2 wet weight, corresponding to 1.64 and 5.51 g C, or 19 and 67 kcal
beneath each square meter. These values are more than an order of magnitude
lower than the values of primary production calculated for these regions:
70-200 g C/m2, i.e., 650-2000 kcal/m2 (Vinberg, 1960). Thus, in the Atlantic
waters of the Norwegian Sea, phytoplankton is to some extent underutilized
by the phytophagous zooplankton.

Table 5. Production of mass planktonic species beneath entire area of
Norwegian Sea occupied by mixed and Atlantic waters, average for 1959-1963
(millions of tons) (Timokhina, 1968).

Mi xed

Atlantic

Maximum annual

Species

waters

waters

production

Calanus finmarchicus

5.58

6.26

16.96

Calanus hyperboreus

0.74

1.42

3.07

Metridia Tonga

1.41

1.34

2.59

Metridia lucens

0.01

0.20

0.44

Pseudocalanus elongatus

0.86

0.38

1.99

Oithona similis

0.05

0.14

0.35

Oithona atlantica

0.07

0.16

0.32

Oncaea boreal is

0.08

0.11

0.29

Aglantha digitale

6.11

24.16

49.90

Chaetognatha

0.92

2.77

6.40

Total

15.83

36.94

--

75

Keeping in mind the similarity of the quantitative development of
plankton in the Norwegian Sea and the Labrador Basin, and also considering
the great extent of the areas of open water in the boreal Atlantic, it is
apparently not a great exaggeration to assume that for the entire boreal
Atlantic area the production of the zooplankton community is 2 to 2.5
times greater than the production calculated for the area of the Norwegian
Sea.

3.3 Planktonic Communities of the Boreal Pacific

In our analysis of the biology of the North Pacific, it is proper
to include in the water area under consideration the actual oceanic
waters and the Far Eastern seas: the Bering Sea, Sea of Okhotsk and
Japan Sea. The unique features of each of these seas, resulting from
differences in their hydrologic modes, latitudinal position and other
factors, cause differences in the makeup of their planktonic populations as
well. Also, the boundary between two biogeographic areas, the northern
Pacific temperate and circumtropical areas, passes through the Japan Sea
(Brodsky, 1957; Zenkevich, 1963). This makes it desirable to analyze
the planktonic communities for each of these seas individually.

Sea of Okhotsk. The planktonic communities of the Sea of Okhotsk
include cold-water and cold-temperate species, and at the very southern
region of the sea adds the oceanic species typical for the warm waters of
the northwestern Pacific. It is most efficient to distinguish three
communities in the plankton of the sea: the oceanic subarctic, oceanic
cold temperate and neritic communities.

The oceanic subarctic community occupies the entire northern portion
of the sea, except for the coastal zone, and extends southward to 56°N,
where it is replaced by the next community. Along the shores of Sakhalin,
this community extends to the latitude of Cape Patience (Mys Terpenia).
The primary components of the zooplankton of this community are: Calanus
glacialis, Metridia ochotensis, Parathemisto libellula and Thysanoessa
raschii . At the end of the summer, the biomass of C. glacialis in the
0-100 m layer in some locations reaches 8000 mg/m3, making up as much as
90% of the entire biomass of zooplankton. In the northernmost region of
the sea, C. glacialis is found everywhere, but is less numerous. It extends
to the south along the shore of Sakhalin together with the cold current, but
plunges to a depth of over 200 m, so that its quantity in the upper produc-
tive layer is not great (Ponomareva, 1961).

Metridia ochotensis is widespread, forms concentrations and is im-
portant in the diet of the Okhotsk herring (up to 45-50% of the diet).
The main concentrations of this crustacean are observed in the northern and
western portions of the sea, the biomass sometimes reaching 1000-5000 mg/m3
in the 0-100 m layer. In the summer and autumn, when the surface tempera-
ture of the water in the southern portion of the sea reaches 15 C, M.
ochotensis is encountered individually, but in the spring the number
becomes quite high (in the southernmost portion of the sea, up to 5000 mg/m3
in the 0-100 m layer) .

76

Parathemisto libellula is common in the waters of the Arctic
structure. This species is eagerly eaten by planktophagous fish, par-
ticularly herring. In the northern regions of the sea, K libellula makes
up to 90% of the diet of the herring. Concentrations of P^. libellula with
a biomass of up to 250 mg/m3 have been reported in the northeastern and
Shantar Is. regions. In the central and eastern regions of the sea, P^.
libellula does not extend further south than 56°N, along the eastern
shores of Sakhalin it reaches as far south as 53°N, gradually submerging
from the surface layer to the 100-200 m layer.

Thysanoessa rashii dominates among the euphausiids. In the fall, it
is encountered in the greatest quantities (up to 2500 mg/m3) along the
shores of Sakhalin and Kamchatka, particularly in the northwestern portion
of the sea (Ponomareva, 1959). In addition to these numerous species,
the oceanic cold-water community includes the copepods Derjuginia tolli and
comb- jelly Mertensia ovum.

The main components of the oceanic cold-temperate community are
Calanus plumchrus, C^. cri status, Eucalanus bungii , Metridia pacifica,
Parathemisto japonica, Thysanoessa inermis, and Th. longipes. C^. plumchrus
IS quite widespread and forms large concentrations in the surface 100 meter
layer. It, together with the euphausiids, is the basis of the diet of the
planktophagous fish. The maximum biomass of C^. plumchrus in the summer and
fall is found in the central region--up to 600-2000 mg/m^ (1959), though
it inhabits the northeastern portion of the sea in large quantities as
well. North of 57°N, the population of C^. plumchrus plummets rapidly.
C^. cristatus is encountered in largest quantities in the southern portion
of the sea, along the Kurile Islands, where its biomass in the 0-100 m
layer may reach 500-700 mg/m3; in the central portion of the sea, it is
not numerous. Eucalanus bungii is also scarce, its biomass reaching 200
mg/m3 (in the 0-100 m layer) only in the southern portion of the sea.

Metridia pacifica extends throughout almost the entire sea, except
for its southwestern portion. The biomass is almost always less than
10 mg/m3, but sometimes reaches 200 mg/m3. The northern boundary of
large numbers of this species, like that of C. plumchrus, is at approximately
57°N.

Thysanoessa longipes and T. inermis basically determine the biomass
of the euphausiids in the Sea of Okhotsk. The former species is encountered
in significant numbers along the coast of Kamchatka, and in the south of the
sea its maximum biomass--up to 3000 mg/m3--is observed in the spring in the
southern portion, in the summer and fall north of 55°N. T. longipes does
not form large concentrations, but is encountered almost throughout the
entire oceanic zone of the sea. The biomass of this species reaches
500-1000 mg/m3 (Ponomareva, 1963).

The warm-water oceanic community in the Sea of Okhotsk is found only
in the zone of influence of the Soya Current, i.e., in the extreme south
of the sea, in La Perouse, Ecatherine and Vries Straits (Brodsky, 1955).
Characteristic species of the community are: Labidocera japonica, L^.
bipinnata, Candacia bipinnata, species of Euchaeta and Corycaeus, Evadne
tergestina, and salps.

77

This same community includes Euphausia pacifica, encountered in

the Sea of Okhotsk primarily near the Kurile Islands (up to 1000 mg/m3),

and in the central portion of the sea only in very small numbers during

the period of greatest warming of the surface waters; apparently, it
does not breed in this area.

The zone occupied by the neritic community is located along the
shores of the sea in a narrow strip extending along the northern shallow
water zones. This community includes larvae of benthic invertebrates and
neritic holozooplankton, consisting primarily of cold-water species.

Japan Sea. The Japan Sea is distinguished by the diverse composition
and great variety of its plankton communities.

Among the copepods, Pseudocalanus elongatus, and particularly
Calanus glacialis. are very important, encountered in the greatest numbers
in the southern portion of the Tatar Strait, extending to the south along
the continent with the cold Primorye Current as far as the shores of
Korea (Meshcheryakova, 1960).

The community of the southwestern Sakhalin waters includes a number
of subtropical, in summer even tropical species and, at the same time,
some northern species (Ponomareva, 1954). A few individuals of the
Okhotsk Metridia ochotensis reach this area through La Perouse Strait.

In the western portion of the sea, the communities of Possiet and
Amur Bays are characteristic (Brodsky, 1957). In Possiet Bay, representa-
tives of subtropical and even tropical fauna are encountered; this
warm-water community populates the waters of the coast of Korea, along
the eastern shore of which a branch of a warm current flows (Uda, 1934).
The community of Amur Bay differs from the Possiet community in that it
includes no tropical species.

In the open portion of the sea, there are two communities: the
northern and southern communities, with their boundary at approximately
40°rNl. Of course, the position of this boundary varies from season to
season and from year to year, depending on the pulsations of the currents.
The 40th parallel is the boundary between the boreal and subtropical plank-
tonic fauna.

The plankton of the Japan Sea is quantitatively rich, the biomass
of plankton in the open portion of the sea reaching 800 mg/m^, along
the coast as high as 2000 mg/m3. The biomass consists of calanids
(C^. plumchrus, C. pacificus, and in the north C. glacialis as well) and
euphausiids (1T[. inermis, Th. longipes, and in the north also Th. raschii ,
in the south--Euphausia pacifica). In some areas, Parathemisto japonica
plays an important role in the biomass of the plankton.

Northern portion of the Pacific Ocean and Bering Sea. In the Bering
Sea, five distinct plankton communities can be differentiated (Brodsky,
1955; Vinogradov, 1956). The southern oceanic community is quite similar in
its specific composition to the oceanic community of the extreme northern

78

portion of the Pacific Ocean, which is natural, considering the hydrologic
similarity of the two areas. The most important characteristic species
are Calanus cristatus, C^. plumchrus are replaced by C. glacial is and
Th. raschii . Certain cold-water species of the latter community descend
with the Anadyr Current to the south to Kamchatka and, together with the
neritic species, make up the western Bering-Sea neritic community, similar
in its specific composition to the eastern neritic community of this sea.
In Anadyr Bay and along the shores of Alaska, there is a neritic community,
characteristic of slightly less saline water. The primary species are
Centropages memurrichi, Acartia clausi , A. longiremis and, particularly,
Podon leukarti (up to 600 indiv./m-^ in the surface waters).

At depths of over 200 m in the southern portion of the sea there is a
deep-water Bering Sea community--derivation of the boreal Pacific Ocean
deep-water community.

The main abundant species of plankton in the Northern Pacific Ocean

(C^. plumchrus, £. bungii , Parathemisto japonica, Euphausia pacifica,

Metridia pacifica beneath the thermocline and C. cristatus above it) form
concentrations with a wery high biomass--up to 2000 mg/m-^.

After the spring rise of £. bungii , C. plumchrus, C_. cristatus,
Thysanoessa raschii and T. inermis to the surface, their biomass in the
0-100 m layer is up to 2500 mg/m^.

The boreal waters of the northern Pacific as a whole are characterized
by a plankton biomass in the upper 100 meter layer on the order of 200-1000
mq/m3. In the south, these waters meet the warm waters of Kuroshio, in
which the biomass of plankton is 10-20 times less (Bogorov, Vinogradov,
1955).

The Kuroshio waters contain a completely different plankton community,
including a significant quantity of tropical species. In the mixing area
between these waters and the boreal waters of the North Pacific, there is
an ecotone community, including both boreal and tropical areas in the
plankton.

79

4. Communities of the Temperate and Cold Waters of the Southern Hemisphere.
(N. M. Voronina)

The population of the pelagic zone of the temperate and polar latitudes
inhabit biotopes with characteristically sudden changes in environment
during the course of the year (see Chapter 1.2 II. 2). As we know, the
essence of the seasonal differences in the pelagic realm is related to
changes in solar radiation which, on the one hand, determine the quantity of
light penetrating the water, and on the other hand, the processes of heat
exchange, causing heating and cooling of the surface waters, formation and
thawing of ice and, as a result, changes in the thermal and density stratifi-
cation. These changes, in turn, influence the delivery of nutrient salts to
the euphotic layer.

Let us take a look at how these factors are reflected in the structure
and functioning of the pelagic communities of the Antarctic and Subantarctic .

4.1 Phytocenes

Factors defining the quantitative development of phytopl ankton. In
Antarctic waters, the concentration of phosphates and nitrates, even during
the phytoplankton bloom and the period of maximum stability of the surface
layer, when their upward travel is hindered, remain higher than in the
winter in the temperate waters of the northern hemisphere. Therefore, they
cannot be considered as limiting factors (Hart, 1934; Bogoyavlenskiy, 1958;
El-Sayed, 1958b). The reason for the exceptional richness of this area in
nutrient salts is the constant renewal of their reserves resulting from the
general character of circulation of the deep water with predominance of up-
welling. Only the decrease in the quantity of silicates, the maximum con-
centrations of which are located deeper than the other biogens, may play a
partial role in the post-maximal decrease in the population of diatoms
(Clowes, 1938; Hart, 1934; Arzhanova, 1974).

The Subantarctic is significantly poorer in nutrients; a decrease in
their quantity is observed as we move northward. However, even in the
Subantarctic, the concentration of phosphates does not drop to a level low
enough to limit the rate of cell division of algae in experiments (Kuenzler,
Ketchum, 1952; Lewin, Guilland, 1963). The addition of a mixture of nutrient
salts to Antarctic and Subantarctic water in experiments did not cause an
increase in primary production (Kabanova et al . , 1974a). It can be said
with certainty that in the Southern Ocean, the concentration of nutrients
does not limit development of phytoplankton. The inverse correlation between
the abundance of phytoplankton and the concentration of phosphates established
by Hardy and Gunter (1935) confirms this opinion quite clearly.

Light is of dominating significance for the vital activity of algae. In
the higher latitudes, the total solar radiation during the course of the
year fluctuates widely. The time of onset of the light season and its
duration differ at different latitudes. The period with minimum solar

80

radiation (below 10 kcal/cni2/month) extends at 60°S from February through
the end of November, at 40°S--only from March to early October, two and
one half months shorter.

As the illumination increases, the rate of photosynthesis increases
up to a certain limit--to the point of light saturation. This point is not
the same at different latitudes (Steemann Nielsen. 1963) or for different
groups of algae (Ryther, 1956). Strickland (1958) reached the conclusion
that the maximum growth of mixed populations of algae occurs with an
intensity of incident radiation of over 0.15 cal/cm2/min, while severe
suppression of growth occurs at over 0.5 cal/cm2/min. Using data on the
mean monthly radiation (Braginskaya et al . , 1966) and the duration of the
light time (Dubovskiy, 1966) to calculate the mean daily radiation, then
comparing it with the conclusions of Strickland, we can see that the light
factor limits the development of algae at the surface at 60°S from May
through August, at 70°C--from April through July. However, in the extreme
south, some areas are freed of ice rather late (Fig. 1?), when the
illumination is beginning to subside, and as a result of this, the period
of optimum light is briefer there.

A mean daily level of radiation sufficient to suppress photosynthesis
is reached at 40°S only in December; further south--it is never reached.
Thus, in the first approximation (ignoring daily changes in radiation), we can

1 xj in I a

^ r ii a-

Fig, 12. Variation in position of northern limit of icepack during the
course of the year at various meridians (after Eskin, 1966).

81

state that over most of the Southern Ocean, the suppressing effect of
this factor does not appear.

The absence of light suppression of photosynthesis is obvious from
numerous data on primary production vertical distribution (El-Sayed,
1968a).

The thickness of the euphotic layer is determined by the position
of the compensation point. In works on primary production, it has been
the practice to consider it to be located at the depth to which 1% of
the incident light penetrates. In the Southern Ocean, this depth varies
during the summer season from 7 to 95 m (Hasle, 1969; El-Sayed, 1968a,
1970b; Steyaert, 1973), depending on the height of the sun over the
horizon and the quantity of phytopl ankton present (Sverdrup, 1953; Hart,
1962). In 78°^ of cases, the compensation point is at a depth of less
than 50 m. This means that the production upon which the population of
the entire mass of the ocean feeds is formed in this very thin layer.

The beginning of the light season is a necessary, but hardly sufficient
condition for the development of phytoplankton. In the spring, when the
entire layer of surface water down to a depth of 100-200 m is well
mixed, cells are drawn away from the surface into the unlit depths,
where respiration predominates over photosynthesis. Therefore, in order
for the development of phytoplankton to begin, it is very important for the
Summer pycnocline to form, limiting the vertical extent of the convection
layer, and for stable stratification to occur, helping the cells to remain
for a longer period of time at the surface.

Changes in the density structure of the water occur as a result of
thawing of ice or the spring rise in temperature over the water area which
is free of ice. Both of these processes lead to development of a layer of
low density, the thickness of which depends on the intensity of wind mixing.
Usually, it increases within the limits of the Antarctic from 10-20 m in
the south to 80-100 m in the north, being 40-60 m in most regions, i.e.,
near the thickness of the euphotic layer. The lower boundary of the
summer transformed water is characterized by an increase in the density
gradient (Makerov, 1956). The vertical stability, reflecting the character
of the change in density with depth, is great throughout the entire surface
layer during the warm season in the high latitudes. Further north, there
is a fairly thick mixed layer. The development of the mixed layer is
characteristically lower and the region with high stability has a greater
longitudinal spread in the Atlantic sector than in the eastern portions of
the Pacific and Indian Ocean sectors. For example, at the 0° meridian,
the value of E'lO^ > 1000 in the 0-50 m layer extends from the edge of the
ice right up to 55°30'S, while at 78°W, it extends only to 65°S, and at 115°E--
to 63°30'S (Ishino, 1963). This is apparently related to the significant
differences in the conditions of formation of the summer stratification.
Since the changes in the density structure of the water between the -2 C
and the +2 C isotherms are determined almost entirely by salinity, differences
in the ice content of the individual water areas become decisive in their
significance (see Fig. 12). In the Atlantic sector, the maximum winter
extent of the icepack reaches 54°S. while the summer ice rim lies at around
70°, but in the eastern parts of the Indian and Pacific Ocean sectors the
ice does not extend as far to the north, and the seasonal movements of the

82

boundary amount to only 4-7°. In the central portion of the Pacific Ocean
sector (120-150°W), where the seasonal movements of the ice boundary amount
to about 10°, high stability is observed over the entire Antarctic zone
(Hasle, 1969). In general features, the boundaries of the maximum extent
of the icepack in winter agree well with the areas of stability of water in
the surface layer. Individual, local deviations are explained by vertical
movement of the water, related to the topography of the bottom (Ishino,
1963) or frontal zones. In the more northern regions, where the summer
stratification is formed only due to heating of the surface layer, its
stability is significantly lower.

The formation of the summer type of density structure of the water
begins in the northern Antarctic zone in mid-October (Fig. 13); in the
Southern Antarctic later. The duration of its existence varies from 6 months
in the region of the convergence to 1-2 months in the high latitudes
(Makerov, 1956).

Seasonal changes in the quantity of phytoplankton. The beginning of
the development of phytoplankton is determined by the increase of light
intensity and the formation of density stratification. What are its
subsequent changes? Long-term observations in the open waters of the
Southern Ocean have never been performed, and our concept of the seasonal
development of the plankton is therefore based on the results of summarization
of materials from cruises. Hart (1942) divided the Antarctic water area into
three latitudinal zones and averaged for each of them by months all the
quantitative data on phytoplankton, based on the concentration of pigments in
Harvey units. These results are presented in slightly altered form in Fig. 20.
In the northern zone, where light stops limiting photosynthesis as early as
September, the increase in the quantity of algae begins in October; the
maximum is reached in December, during the period of sharply increasing
stability of the surface layer; in March, the late-summer minimum occurs;
in April, a second maximum, significantly less than the December maximum, is
observed, followed by a sharp decrease, accompanying the autumnal mixing.
From north to south, the length of the period of vegetation decreases, the
time of the peak is increasingly delayed (January-February), and the
second maximum drops off in the intermediate zone, then disappears completely
in the southern zone. The correctness of these concepts, in their general
features, has been confirmed repeatedly (Vinogradov, Naumov, 1961; Hasle,
1969; Steyaert, 1973; Voronina, Zadorina, 1974).

Extremely sparse materials are available for the Subantarctic. The
vernal maximum of plankton in the Atlantic sector is observed there primarily
in October-November (later in the south than in the north); the second peak,
apparently, occurs in March-May. In the Pacific Ocean sector, where the
boundary of the Subantarctic is shifted far to the south, the bloom is
observed in late December (Cassie, 1963; Hasle, 1969).

This picture is quite schematic, and the limits of possible fluctuation
of individual indices are great. Among the factors defining the onset of
biologic spring (according to Bogorov, 1938), only changes in solar radiation
are constant with respect to time. The depth and intensity of the pycnocline
depend on the force and duration of the wind (Makerov, 1956); a decrease in
temperature may cause ice formation in the high latitudes even in mid-summer;

83

Fig. 13. Seasonal changes in the
stability of the 0-100 meter layer
in the northern region of the
Antarctic (Currie, 1964).

M It XT !

IV IS
M 7

the configuration of the coastline modifies the drift of the ice, causing
its accumulation on the eastern sides of projecting parts of the coast, and
milder conditions on their western sides (Yeskin, 1969); the specifics of
the edge of the shelf and of the deep water circulation lead to the fact
that in some places the southern waters become free of ice earlier than
the more northern. All these peculiarities disrupt the latitudinal
sequence of the hydrologic and biologic seasons. Along with the main
seasonal maxima of phytoplankton, other maxima may exist, e.g., at the
edge of the ice or near icebergs (Kozlova, 1964; Steyaert, 1973; Voronina,
Zadorina, 1974). The time of the bloom may change from year to year in
the same place. For example, at 20°E in January of 1967, the maximum
population of diatoms was located some 6° further north than in January
of 1965. Such deviations make the average picture of seasonal changes in
the quantity of phytoplankton smoother; therefore, in order to judge the
true amplitude, measurements must be made during the extreme periods.
There are little data suitable for comparison, due to the great variety
of methods which have been used for collection and processing of phytoplank-
ton and for the presentation of results. Therefore, here and below, in
order to describe the quantity of phytoplankton, in addition to the
number of cells, we will also use information on plant pigments, and--
at times--on primary production.

In the winter, beneath the ice, there ixv& practically no algae. In
the open water in the Antarctic, the concentration of plant pigments is
about 50 Harvey units per cubic meter, the mean monthly quantity of
chlorophyll "a" at the surface is not over 0.1 mg/m^, decreasing in places
to 0.01 mg/m^ (El-Sayed, 1970a). During the period of the phytoplankton
bloom in the Antarctic waters, the number of diatoms at the surface reaches
1-4-105, and even 10^ indiv. /liter (Fukase, 1962; Zernova, 1970; Steyaert,
1973: Marumo, 1957; Kozlova, 1964). The mean number of algae in the upper
100 meter layer is on the order of 10*^-105 indiv. /I iter (Sanina, 1963;
Steyaert, 1973). The concentration of plant pigments during this time may
exceed 5-10'^ Harvey units per cubic meter (Hart, 1942); the concentration of
chlorophyll "a" exceeds 15, reaching 123 mq/m^ (El-Sayed, 1968a, 1970a, b);
the biomass of wet seston, strongly dominated by phytoplankton, may reach
27 g/m3 (A. I. Ivanov, 1959) and 56.5 cm^/m^ (Marumo, 1953). Even beneath
non-thawing ice, at the time of breakup of its lower surface, the popula-
tion of the Phaeocystis reaches 1 million cells/liter (Bunt, 1964b). In the
Subantarctic at 20 E, during the bloom, the population of diatoms in the
upper 100 meter layer has been observed as high as 3.4-105 cells/liter
(Steyaert, 1973), to the southeast of the Falkland Islands--! .5-lo7 cells/
1 iter.

84

These data show that the scale of time changes in the quantity of
phytoplankton is very great. Unfortunately, there are but limited
materials available for a judgment concerning the length of the maximum
period. In the coastal waters near the Southern Orkney Islands, the
time of maintenance of high concentration of chlorophyll "a" is about 3
weeks and the high indices of primary production last for about 2 weeks
(Home et al . , 1969), while in the area of Mirnyy, the duration of the
period of intensive production was less than 10 days (Klyashtorin,
1964). All of this indicates the very short duration of the periods of
high concentration of phytoplankton. The drop in phytoplankton occurs
during the period with a high content of nutrients in the water, and
cannot be explained by exhaustion of them. Probably, the reason for the
phytoplankton drop is the increased consumption of algae by the developing
generations of herbivores (Hart, 1942; El-Sayed, 1968b; Home et al . ,
1969). However, no comparison of the rates of production and consumption
has ever been performed; the content of trace elements and vitamins has
never been determined, although the influence of these factors on the
development of algae may be very great (Provasoli, 1963; Belser, 1963).
Therefore, the concept of the connection between the seasonal decrease
of phytoplankton and the press of herbivores is as yet but a hypothesis.

Vertical distribution. During the production period, the maximum
of phytoplankton population is located in most cases in the upper 10 or
20 meter layer (Hart, 1942; Hasle, 1969). It lies frequently not at the
surface, but rather at a depth of 5-10 m. The quantity of algae decreases
more or less rapidly with increasing depth below this layer. Usually, a
clear dependence is observed between the degree of the density stratifica-
tion of the water and that of the phytoplankton (Hasle, 1969). With
high stability of the surface layer, the algae are found in the uppermost
level, and most of their populations are in the euphotic zone, where
illumination is optimal. In the Southern Ocean, where nutrient salts
are not limited, we should not expect any negative influence of stability
on the production at the end of the season, as occurs in the northern
temperate regions (Riley, 1946). With stronger vertical motions of the
water, the distribution is more uniform, conditions of photosynthesis
deteriorate and the quantity of phytoplankton decreases. This is observed
in the area of the Antarctic convergence (El-Sayed et al . , 1964; El-
Sayed, Mandelli, 1965; Mandelli, 1967) and in places with intensive
upwelling of water, e.g., in the region of the cyclone near the divergence
to the north of Enderby land (Beklemishev, 1959), but not along the
entire zone of the divergence, as has been sometimes thought (Beklemishev,
1960; Kozlova, 1964). The influence of factors facilitating or preventing
an increase in productivity of phytoplankton is felt through the influence
on its vertical distribution.

In many places, particularly in less stratified water, more than
half of the population is found in the hypophotic zone (Mandelli, Burkholder,
1966; Home et al . , 1969; El-Sayed, Dill, 1972). Sometimes even the
maximum population is located deeper than the compensation point. This,
apparently, is a result of its submergence from the higher levels, and
indicates a late stage in the seasonal succession.

85

Summarized data on the distribution of the population of individual
groups of algae are presented in Table 6. The greatest tendency to remain
near the surface layer is observed in the flagellates and diatoms. This
tendency is significantly less in the dynoflagellates, among which are
many obligate heterotrophs, and minimal in the Coccolithophoridae. The
distribution is somewhat less clear in the Subantarctic: The surface layer
contains a smaller fraction of phytoplankton, the population maxima are
located deeper.

Table 6. The frequency of occurrence of the population maxima of various
groups of algae (% of number of stations) in different layers in the
Pacific sector of the Southern Ocean in December 1947-February 1948 (after
Hasle, 1969).

Group

Zone

0-25

Depth
26-50

, m
51-75

76-100

>100

Maximum
depth

Diatoms

A

SA

72.3
65

12.5
10

7.5
5

7.5

0

0
20

98
162

Dynoflagellates

A
SA

62.5
50

27.5
30

7.5
15

2.5
5

0
0

98
76

Monads and
Flagellates

A

SA

82.5
66.5

12.5
28.5

2.5
5

2.5
0

0
0

92
71

Coccolithophoridae

A
SA

50
39

25
11

0
39

25
5.5

0
5.5

100
182

Note: A = Antarctic; SA = Subantarctic.

Ice flora. The vegetation of algae is possible not only in the open
water, but also in the ice. There are two maxima of development of ice
phytoplankton: the fall maximum, appearing on the bottom surface of the
ice in March-April when the thickness of the ice is about 30 cm, and the
spring maximum, arising in October at a depth of more than 1 m (Hoshiai,
1972). The ice flora is usually localized in the water-snow and congelation-
ice layers (Oradovskiy, 1973). The composition of diatoms differs in these
two layers and, apparently, is determined by the time of settlement. An
eponic group is distinguished, including attached species of the genera
Pleurosiqma, Nitzschia, Amphiprora, Fragilaria, and a permanently plank-
tonic group, living among the ice crystals: Biddulphia, Coscinodiscus,
Asteromphalus (Bunt, Wood, 1963). The main group of this algae are diatoms.
Their number in this biotope may be very high: up to 5-40-106 cells/1,
while under the ice it is extremely low (Bunt, 1963, 1968). The ice
community lives under extreme conditions: The content of nutrient salts is

86

lower than in the open water (Oradovskiy, 1973), illumination amounts
to only a few hundredths of 1% of the illumination on the surface (Bunt,
1968). Therefore, only forms adapted to weak light can live in the ice.
Actually, the alqae liberated from the ice manifest the maximum photo-
synthetic activity at an illumination level of 103 Ix (Bunt, 1968), 1/10
that of planktonic representatives of the group (Ryther, 1956). This
can be reflected in the productivity of the population. Under natural
conditions, the time between divisions in diatoms averages 6 days (Bunt,
1968). However, due to the absence of sinking, even with this extremely
low development rate, a quite detectable increase in population occurs
over the vegetation season. This factor, plus the high content of
chlorophyll, resulting from the insufficiency of light, has led several
authors to consider the ice flora to be of high significance in the
synthesis of organic matter. This is not true. But doubtless, its
influence on the pelagic community is quite great. The area of annually
thawing ice is some 18 million km^ (49% of the area of the Antarctic zone).
As it breaks up, a tremendous quantity of algae enters the water. Many
species become true plankters and continue their existence in the water.
This intensive "seeding" of the water area as it opens from the ice is
of great ecologic significance, facilitating a rapid onset of the bloom.

Regional differences in the quantity of phytoplankton. Are there
differences among regions of the Southern Ocean in terms of abundance of
phytoplankton? It is difficult to answer this question, due to the
asynchronous appearance of the definite stages of the annual cycle and
the briefness of the bloom. A comparison can be made only on the basis
of materials collected by the same method, for water areas, the plankton
of which is in the identical state of seasonal development, preferably
for the period of the maximum or on the basis of multiannual studies.
In spite of the limited nature of the available data, some general concepts
have been developed with respect to this question.

The neritic regions, both of the Antarctic and of the Subantarctic
zones, are richest. The mean abundance of phytoplankton in the 0-100 m
layer during the period of the maximum near South Georgia Island is more
than 10 times the mean abundance in the remaining water area south of
the Antarctic convergence (Hart, 1942). Since this region was among the
first studied, information on it was applied to the entire ocean, and the
initial estimates of productivity of the Antarctic were thus far too high.
Averaging of a large volume of data on Pacific and Atlantic sectors of the
Southern Ocean have shown that, on the whole, the neritic waters are
approximately 5 times richer than the oceanic waters (El-Sayed, 1970a).
The reason for this is the abundance of trace elements and the intensive
consumption of phytoplankton more intensive in comparison to the open
ocean. Within the oceanic waters of the Antarctic, there are significant
differences between the northern and southern zones. Many observations
indicate a significant increase in the maximum in the southern latitudes,
particularly in the waters near the ice. It is here that record concen-
trations of algae have been observed (Kozlova, 1964; Walsh, 1969; A.I. Ivanov,
1959; Hasle, 1969). These differences are apparently based on an increase
in the stability of the southern waters, caused by thawing, as well as
the "seeding" of the pelagic zone by the flora liberated from the ice
(Hart, 1934; Bunt, 1964a). Therefore, the boundary of the rich zone should

87

apparently more correctly be considered to be not the Antarctic divergence
(Kozlova, 1964), but rather the northern limit of the icepack.

Many authors have affirmed the relatively low quantities of
phytoplankton in the Subantarctic zone in comparison to the Antarctic
(Boden, 1949; Beklemishev, 1960; Kozlova, 1964; El-Sayed, 1970a). However,
some data indicate that inverse quantitative relationships do exist
(Hart, 1934; Cassie, 1963; Hasle, 1969; Steyaert, 1973). The quantity
of algae during the peak period in the Subantarctic can reach the same
order of magnitude as in the lower Antarctic. The opinion of the poorness
of the Subantarctic has resulted apart from the fact that this area is
usually explored by expeditions which have come in to study the Antarctic
summer, and they crossed this zone after the phytoplankton bloom; compari-
sons have been conducted for waters in different stages of plankton suc-
cession.

The data presented reflect the differences in the individual water
areas only in terms of the quantity of phytoplankton during the period
of abundance. Productivity estimates might be essentially different,
first of all due to the different duration of the vegetation season.
Attempts to determine this quantity approximately on the basis of the
data presented by Hart (1942) on the mean annual quantity of plant
pigments show that the southern zone is 207o poorer, the northern zone
20% richer, than the intermediate zone. The inshore waters of South
Georgia are four times more productive than the northern zone, within
which this island lies.

Composition of flora and its seasonal changes. The flora of the
Southern Ocean has been studied quite insufficiently. At the present
time, some 180 taxons of diatoms, 70 species of dynoflagel lates, five
coccolithins and five sil icoflagel lates have been listed (Hasle, 1969).
We can use the data of Hasle (1959), who has considered the area of dis-
tribution of 77 species (in addition to the broadly distributed species)
to judge the degree of isolation of the flora of individual zones. Among
the species she studied, the number found in the Antarctic and Subantarctic
is practically the same; 30% of the species inhabit the Antarctic alone;
some 27% of the species are not seen in the Antarctic; all of them,
except for one Subantarctic endemic species, being invaders from the
northern waters. The low degree of endemism of the Subantarctic flora in
comparison to the Antarctic also follows from analysis of the distribution
of dynoflagellates (Balech, 1968).

A predominant role of diatoms is characteristic for the Southern
Ocean. Their number in the Subantarctic represents up to 80%, in the
Antarctic up to 99.9% of the species present (Hart, 1934). The composition
of phytoplankton is quite uniform: Almost always (96% of cases), one
or two species make up more than half of the total population (Marumo,
1953). Among the dominant species are: in the Subantarctic, Chaetoceros
neglectus, Nitzschia "barkleyi ," Coccol ithus huxleyi , in the lower
Antarctic--Ch^. dichaeta, Ch. neglectus, Fragi lariopsis "nana ," N^.
closterioides, in the higher Antarctic--F. curta, £. cyl indrus, and H_.
subcurvata . The variety index of flora Tafter Margalef) is not great,
increasing from 2.4-3.0 in the southern zone of the Antarctic to 3.2-3.7
in the Subantarctic (Hasle, 1959).

The use of the fluorescent microscope in recent years has changed
many of our concepts of the composition of phytoplankton in the Southern
Ocean. It has been shown that, considering the microflagel lates , its
total population reaches I-5'IO^-^ indiv./m^, with nanoplankton making
up as much as 99% of the total number of cells (Walsh, 1969). However,
the distribution and duration of existence of these concentrations are
still not known.

The composition of plankton changes with time. Extensive cruise
collections (Hart, 1934) have allowed an attempt to be made to classify
the most abundant species in accordance with their seasonal abundance
and to distinguish: vernal forms; forms which rrake up the maximum in
the spring, but are retained in large numbers throughout the entire
season; species which participate in the formation of the spring and fall
maxima, and species which form the maximum in late summer and fall.

Further investigations have resulted in the detection of a succession
in species composing the peak during its seasonal shift to the south. In
addition to species which are present everywhere, others have been found
which are significant only in the northern or only in the southern latitudes
(Steyaert, 1974). Forms have been described which increase their number
during the decrease in the total quantity of phytoplankton. However, in
spite of the great qualitative variety of flora, we should not expect to
find a rigid succession of dominant forms, particularly since the degree
of connection of certain species of algae with others through the metabolite
path varies from obligate symbiosis to complete independence (Lukas,
1964).

Let us emphasize the most important specifics of the phytoplankton
of the Southern Ocean: great amplitude of quantitative changes during
the course of the year and regional differences in maximum abundance;
brevity of the maximum; a general shift in the zone of the bloom during
the course of the season from the north to the south; significant local
variations in the time of onset of the maximum, related to local hydrologic
and meteorologic conditions; a seasonal succession of the composition
of the phytoplankton.

4.2 Zoocenes.

Life cycles. The main peculiarity of cold-water ecosystems, the
discontinuity of the process of primary production, has its maximum
influence on the mode of life of the main groups of animals in the Southern
Ocean. The cycles of herbivorous interzonal copepoda of the Antarctic
and Subantarctic occur practically identically and consist in successive
changes of the physiologic state, abundance, age composition, vertical
structure and distribution of the numbers of the populations. During
the biologic spring, sexually mature crustaceans accumulate in the narrow
surface layer, richest in phytoplankton. Their total number during this
period is usually not great, but local concentrations may be significant.
They feed, mature and breed here. All representatives of the families
Calanidae and Eucalanidae are characterized by a broad feeding spectrum,
and in all stages of their development, begltining with the first copepodite
stage, they consume all species of algae measuring from 5-300 pm in diameter.

89

The number of eggs produced by the females is apparently directly dependent
on their food supply, i.e., on the Quantity of algae present during the
spawning season. The buoyancy of the eggs of the copepods is negative,
but some excretions of the phytoplankton increase the viscosity of the
water and slow the sinking of the eggs (Maloney, Tressler, 1942). The
nauplii emerge in the uppermost layers of water and a high concentration
of the population, the core of which is usually in the upper portion of
the mixing layer, is characteristic for early stages of the development
of the generations. The total number of individuals reaches its maximum
during this period. Later, as the crustaceans grow, they gradually
disperse vertically: The older stages begin to sink into the depths,
and at first the lower boundary, then the upper boundary of their habitat
move downward. Therefore, in the summer the cores of abundance of
individual copepodite stages typically go deeper as they become older
(Voronina, 1970a, 1974).

As time passes, the populations are significantly reduced in number,
but, due to the intensive growth of the individuals, their total biomass
increases, reaching its maximum in the surface layer during the period
of dominance of the fourth and fifth copepodite stages. Older stages,
having accumulated large droplets of fat, begin to leave the euphotic
zone and disperse through the mass of the water. The number maxima of
the individual species are observed in the winter at a depth of 750-1000
or 250-750 m (Mackintosh, 1937: Andrews, 1966). The wintering populations
of copepods over most of the aquatorium are characterized by predominance
of the fourth and fifth copepodite stages. During this period, the
crustaceans do not feed and utilize the summer fat reserves. The popula-
tions retain the seouence of individual copepodite stages along the
vertical of late summer: younger copepodites are located higher than
older. However, in spring, as the rise begins, a restructuring of the
vertical distribution occurs, since the mature individuals which move more
rapidly than the others, catch up with and even pass first and fifth, then
the fourth stage copepodites, after which the fifth stage copepodites pass
the fourth stage copepodites. As a result, a structure is produced which
is typical for the final stages of migration, in which the older stages
are followed by younger stages from the top downward. The vertical spread
is greatly reduced, reaching its minimum during the spawning period. In
general features, the changes in the sequence of copepodite stages along
the vertical and of quantitative distribution of species numbers by
depth can be represented as in the diagrams below (Figs. 14 and 15). The
individual stages of this cycle differ in their age composition and total
numbers of populations.

This type of restructuring has been seen for Calanus propinquus, C.
simil 1 imus , Calanoides acutus , Rhincalanus gigas , as well as Pareuchaeta
antarctica and Metridia gerlachei , in which it is somewhat complicated
by the daily vertical migrations. Apparently, these cycles are charac-
teristic of all interzonal copepods which breed in the surface layer.

One important peculiarity of the annual cycles of planktonic animals
is the asynchronism in occurrence of identical stages of these cycles in
various latitudinal zones. The rise to the surface, breeding, attainment

90

fi:'!}

Jfff

S 4(

J7 o <r

^ ^M

IF

JY JT

IT

Fig. 14. Changes in vertical structure of population of interzonal
species during the annual cycle. Roman numerals show position of median
of hemi populations of individual copepodite stages. 1, Winter;
2, Beginning of spring migration; 3, End of migration, spawning;
4, Development of new generation; and 5, Beginning of fall sinking
(Voronina, 1975).

Fig. 15. Seasonal changes in vertical
distribution of interzonal species
population (Voronina, 1972).

of a certain age, and maximum biomass and the downward migration occur
earlier in the northern latitudes and later further south (Voronina, 1969,
1974; Voronina, 1970). Deviations from this sequence are related to
hydrologic peculiarities which define the deviations in the time of
beginning of intensive phytoplankton production (Voronina, 1975). The

91

time difference of the onset of individual stages may be quite great. For
example, in the zone of the Antarctic convergence, the breeding of
Calanoides acutus occurs in November, of Rhincalanus gigas--in December,
while in the southern latitudes they occur in February and late March,
respectively. As a result, as we move along a meridian, we can observe
sequential changes in the age and space structure of the populations and
their abundance, analogous to their changes with time.

The duration of the cycle differs for different species. Populations
of C^. acutus and C. propinquus follow a single generation almost every-
where; R_. gigas in the southern latitudes, with the short vegetation
season, does not succeed in completing its development in a single summer,
and it is extended over two years (Voronina, 1970). The Subantarctic
C. similis and C^. tonsus, apparently, are bicyclic. The specific differ-
ences in the development of copepoda primarily concern the time of the
spring ascent to the surface and breeding, as well as certain details
of the vertical distribution: depth inhabited by the wintering group,
absence or presence of daily migrations and their scale.

Another important group of the pelagic population is the euphausiids.
The cycle of the most numerous species of this group, Eupheusia superba,
living south of the Antarctic convergence, has been most fully studied.
This crustacean, apparently, can breed in any region of the Antarctic
where spawning accumulations are formed, even around South Georgia Island
(Mackintosh, 1972; Makarov, 1972). The eggs are spawned in the upper
layers, then gradually submerge to great depth, as much as 2000-3000 m
(Fraser, 1936; Bargmann, 1945; Marr, 1962). During the sinking their
cleavage proceeds. As a result the deeper the eggs, the more advanced is their
development. The emerging nauplii begin active ascent during which
development continues. The larvae usually reach the surface water in the
first calyptopis stage. Only here do they begin active feeding. The
morphogenesis of £. superba is Mery variable (Fraser, 1936). Five different
paths of ontogene?is of the crustaceans have been described. The path
followed by development is apparently determined by the environmental con-
ditions (Makarov, 1974).

In the surface water the larvae perform vertical migrations, the
amplitudes of which decrease with increasing age (Marr, 1962). However,
Simultaneously with this, the entire population tends to rise and is
concentrated in the upper 25 or 50 meters of water (Makarov, 1974). The
seasonal submergence into the deep water does not occur for this species.
The biologic sense of this cycle is obvious: The submergence of the eggs
and early larvae below the layer where they can be eaten by mature
euphausiids helps to preserve the population (Marr, 1962; Pavlov, 1969).
During the first year of life, the crustaceans complete their larval phase
of development; ;during the second year the juveniles feed and grow;
during the third year, the crustaceans mature and breed. In case of
unfavorable conditions, the cycle can extend to four years; this is
characteristic of crustaceans in the most southern Antarctic regions
(Makarov, 1972).

Varying their location in the great range of depths, E_. superba is
subject to the influence of various hydrologic factors which, to a

92

significant extent, determine the character of its distribution in
various developmental stages. The early larval stages of this species,
in contrast to the mature stages, occur in a rather limited water area,
including the East Wind Drift and the Weddell Sea circulation. No other
of the numerous species of the Antarctic have such distribution. All
other biologic boundaries in the pelagic zone coincide with the zones of
physical boundaries or are parallel to them. The picture of the Quantita-
tive distribution of £. superba , however, shows clear asymmetry and
brings up the question: What prevents the development of the larvae
over the broad aquatorium of the West Wind Drift in the Indian and Pacific
Ocean sectors, the ecologic conditions in which are practically the same
as those in the Atlantic? At the present time, this factor has but one
explanation. Obviously, the depth of submergence of the eggs and, con-
sequently, the distances which the larvae must travel as they rise to
the phytoplankton-rich waters, are different in different regions and
are inversely dependent upon the density of the water. In the shelf
zone, filled with cold water, submergence occurs more slowly, and even
if the eggs fall to the bottom, the larvae emerge in lesser depths and
come to the surface in earlier stages than in the oceanic zone (Marr,
1962). We can assume that there is a depth limit which the nonfeeding
larvae can travel on their return path upward, and that individuals which
descend to greater depths die without reaching the layer of photosynthesis
(Voronina, 1974).

Obviously, the vertical structure of the water has a very significant
influence on the depth of submergence of the eggs; in particular, the
transition from the deep water mass to the denser bottom water should be
accompanied by a slowing or complete stoppage of movement, as is observed
in the sinking diatoms (Wood, Walsh, 1968). A comparison of the topography
of the upper boundary of the bottom water mass and the quantitative dis-
tribution of the calyptopes of E^. superba has yielded interesting results.
The Antarctic bottom water mass is formed as a result of cooling and
freezing of shelf water with its subsequent mixing with the deep water and
sliding downward along the slope (Mosby, 1934). therefore, the depth
of its upper boundary increases rapidly from the continent to the north.
Only in the Weddell Sea is there a dome-shaped elevation of this water,
caused by the cyclonic circulation (Klepikov, 1963). It has been found
that the location of the calyptopes practically coincides with the zone
where the denser water lies at a comparatively shallow depth--around
1800 m. This depth corresponds approximately to the maximum depth of
winter sinking of the interzonal copepoda and, probably, is close to the
maximum distance which many interzonal organisms can travel in their
seasonal vertical migrations. This gives us reason to believe that the
breeding of E^. superba can be truly successful only in regions where the
upper boundary of the bottom water mass is located relatively high. In
this area there are two large circulations (the East Wind Drift and
the Weddell Sea circulation), holding most of the rising crustaceans
within their boundaries. Therefore, the maximum population of all stages
is found in these waters, and only a portion of the population is carried
out beyond them. The process of gradual expansion of the habitat as
the generation develops has been clearly traced (Fig. 16) in larvae
living in the surface layer: The boundaries of their distribution shift
to the east from month to month (Marr, 1962).

93

Fig. 16. Distribution of larvae of Euphausia superba on the surface,
1, Summer; 2, Winter (Marr, 1962, simpl i fied ) .

Expatriation to the north, to South Georgia Island, occurs both as
a result of direct penetration of water from the Weddell Sea with the
current flowing along the arc of the South Sandwich Island, and as a
result of episodic transfer of surface water through its boundary zone
(Solyankin, 1969; Maslennikov et al . , 1971; Yelizarov et al . , 1973).
The transfer of crustaceans from the East Wind Drift is possible in
areas where the branches of the circulations which form it turn to the
north (Treshnikov, 1964). The movement of the surface water in this
direction has been described on the basis of satellite observations of
iceberg drift (Tchernia, 1974). As a result, a portion of the population
of E^. superba is scattered over the broad spaces of the Antarctic
beyond the limits of its main area of distribution. Such representation
agrees well with materials on the Quantitative distribution of krill
(Marr, 1956, 1962): Massive accumulations of crustaceans are related
to the East Wind Drift, the circulation of waters of the Weddell Sea,
regions of Bransfield Strait and South Georgia Island, i.e., they are
similar to the distribution of calyptopes, but somewhat broader. New
data (Mackintosh, 1973) have not carried us beyond the framework of this

94

Fig. 17. Change in the position of the regions of commercial whaling
during the course of the summer (according to pre-war data). 1, November;
2, January; 3, March (Mackintosh, 1973, modified).

concept. A slightly different
of mul tiannual visual registra
Mackintosh, according to which
ring, moving southward in the
furthest northern position is
position--in March. It agrees
accumulations of whales (Fig.
in the northern latitudes is r
However, £. superba swarms in
existence of swarms is longer,
i.e., the presence of swarms i
plankton bloom (Pavlov, 1969,
maxima ring, as shown above, c
krill swarming. This indicate
primarily a reflection of the
can hardly be considered as an

picture is yielded by the summarization
tions of surface swarms, undertaken by

the "krill zone" is a narrow circumpolar
summer, following the retreating ice. Its
observed in December, its most southern

well with the distribution of commercial
17); therefore, the disappearance of swarms
elated by this author to consumption,
the intervals between feeding and the

the more abundant the phytoplankton;
s most typical of the period of phyto-
1974). The position of the phytoplankton
hanges with time analogously to the zone of
s that the picture drawn by Mackintosh is
character of distribution of E. superba and

indication of the abundance of the species.

95

although, in principle, there is doubtless a decrease in the abundance
of the crustaceans in feeding zones.

The peculiarities of the biology of other Antarctic and, particularly,
Subantarctic euphausiids have been much less thoroughly studied. The
second most massive species is Thysanoessa macrura, widespread in the
Antarctic and extending into the southern Subantarctic. Judging from
the occurrence of the early stages, breeding of this species occurs
between October and February, the duration of the cycle being one year
(Ruud, 1932; Rustad, 1934; K. N. Pertsova, 1975). The population
maximum is found in the upper 100 meter layer. The regions of greatest
abundance of both mature individuals and larvae are extended along the
Antarctic convergence and divergence (Lomakina, 1964; K. N. Pertsova, 1975)
Euphausia triacantha has a similar distribution, but the primary con-
centrations of this species are clearly confined to the convergence zone
(Baker, 1959). This species performs great diurnal migrations, sub-
merging during the day to depths of over 250 m, and has a two-year cycle.
The duration of life of E_. frigida is the same.

The third important group of herbivores is the salps. Of these,
the cycle of Sal pa thompsoni has been most thoroughly studied (Foxton,
1956). It is very common to the south of the Subtropical convergence.
The range of habitat extends down to 1500 m, the maximum population
being found in the surface water. There are daily migrations. During
the course of the winter, the juvenile asexual forms grow, developing
stolons which carry the buds of sexual zooids. Early in the spring, the
fully formed sections of the stolons begin to separate. From October
through February, their number increases by a factor of more than 10, but
then decreases once more in March. As the colonies grow, they submerge
into deeper water. In each, one fertilized egg develops which, after
completing morphogenesis, is liberated at the end of the summer and
continues to develop in the form of an individual, supplied with a food
reserve and already having a primordial stolon. The development of the
salps in the deep layers occurs more slowly and by the beginning of
spring, some individuals are still in the early stages of development.
Therefore, throughout the summer the population consists of organisms of
varying ages.

The most numerous group of predators--the chaetognatha--is also
interzonal . Most abundant are Eukrohnia hamata , Sagitta gazellae and
S_. marri . The annual cycle is best known for S^. gazellae (David, 1955).
Breeding occurs in the deep zone from spring to fall. The region of its
greatest intensity shifts as the season progresses from the northern
Subantarctic to the south. The spawned eggs float into the upper
horizons: Hatching occurs at a depth of about 250 m, subsequent develop-
ment--in the 0-100 m layer. In the winter, the Sagitta grow by
approximately 5 mm per month, somewhat more rapidly in the spring and
summer. Juveniles, as they mature, gradually submerge, the more mature
individuals being located deeper. Mature individuals are found only at
depths of 1000-1500 m. The duration of one generation is one year. The
development of other species differs only in details. All species perform
seasonal migrations.

96

The predaceous Hyperiidea Parathemlsto gaud1chaud1 begin to breed
in September. Each female spawns several times, after which some of the
females die, while others survive to the fall and breed again. The
juveniles appear in September, reaching their maximum number in December.
Due to the long period of breeding, the young crustaceans are present in
the plankton as late as June. Some of the larger females may survive
a second winter and breed again (Kane, 1966).

A comparison of the mode of life of the most numerous plankters
shows great similarity with respect to the most important characteristics:
Breeding (or the time of its maximum intensity) in all species occurs in
the spring or summer; feeding and growth of the juveniles occur in the
Surface or subsurface layer; most of the population perform daily,
seasonal and/or ontogenetic vertical migrations, removing them from
the surface waters.

This similarity of cycles in different groups of organisms is a
result of the peculiarities of the environmental conditions in the
Southern Ocean. The discontinuity of the process of primary production
makes it necessary for numerous species to spend the vegetation season in
the euphotic layer or directly beneath it. Here, the herbivores find
the maximum algae and can grow rapidly, breed and create reserves of
fat for the long winter, while the predators feed on the concentrations
of copepoda and euphausiid larvae. However, if the entire life cycle
were spent in the surface waters, there would be the danger of loss of
a significant portion of the population by being carried by meridional
Currents away from the breeding zone. Any vertical migration decreases
the effect of this transfer, while scattering into the deeper water
makes it harder for predators to decimate the population. The specifics
of the biotope have resulted in the predominance in the zoocene of the
cold-water pelagic zone of nonspecialized interzonal species, occupying
"large" niches in comparison to those of the tropical plankters.

Another important feature of the life cycle of the zooplankters is
their great plasticity. This is manifested as the variable duration of
development of different individuals (P^. gaudichaudi , R. gigas, E^.
superba) , as well as the mixed age composition of populations (Salpa
thompsoni , P_. gaudichaudi ) , and the variety of possible paths of
morphogenesis (E. superba"). The plasticity of cycles allows the species,
depending on environmental changes, to change their development, which
serves as a sort of insurance in case of excessively severe perturbations.

The differences between cycles consist in the greater length of the
breeding period of most predators in comparison with the existence of
high concentrations of their prey. The time of breeding and the range
of vertical distribution is also diverse in various species. At first
glance, these differences seem to be secondary in nature but, as will be
demonstrated below, they are of primary significance for the structure
and functioning of the community.

The quantitative distribution of individual species is influenced
by a variety of factors, among which we can distinguish two important
groups: temporal and regional. The amplitude of fluctuations in the

97

number of individual populations during the course of the year may be very
significant. It is particularly great for plankters with nonoverlapping
generations, including all of the interzonal copepods. The numbers of
the new generation are maximal after hatching. Subsequently, their number
decreases due to consumption and natural death. At the same time, as
the juveniles develop, the relative fraction of older individuals
increases. On the average, during the time of the development of the
population from the stage of domination of early copepodites to domination
of the fourth or fifth stage, the number of crustaceans beneath each
square meter decreases by a factor of three or four, then still more
sharply over the next winter. It follows from this that, in addition to
the regional aspects of distribution, any survey reflects the seasonal
aspects, the differences resulting from disagreement in phases of the
cycle overlapping with local differences. This is important to consider
in any comparative evaluation of the abundance of a given species in
various latitudinal zones or areas with different ice regimes. A comparison
of areas with identical age composition of individual mass species shows
that the number of crustaceans may vary by a factor of more than 20,
creating a rather variegated picture. It is based upon factors deter-
mining their distribution. The former include the number of organisms
in the spawning pool and the feeding conditions during the period of
breeding and growth. The distribution of the spawning pool of inter-
zonal animals depends on the abundance of individuals of the previous
year's generation, descending from the surface waters, and on their
subsequent transport by deep water currents. Since the rate of transport
by deep water currents is slow, it usually results in no significant
changes. Data on the distribution of Calanoides acutus (Andrews, 1966)
and the total biomass of zooplankton (Foxton, 1956) shows that the
character of distribution remains practically unchanged during the course
of the winter months. Only in the central Atlantic sector, where the
deep waters, compensating for the great efflux of bottom water, have
an elevated southern component in their velocity vector (Arsen'yev et al.,
1975), is significant southward shift of the wintering pool of plankters,
as well as penetration of subtropical species far into the Subantarctic,
and of Subantarctic species into the Antarctic, possible (Andriyashev
et al . , 1973; Voronina, 1975). In addition to this, some changes in
the deep water plankton occur in the zones of divergence, to which the
meridional components of the currents "carry" the animals from the
nearby water areas. Although these currents are weak, over the course
of the long winter, the concentration may increase significantly in
comparison with neighboring sections (Voronina, 1966b). In general,
the abundance of the wintering pool varies less than the abundance of
summer population (Voronina, 1975).

The amount of food available for the ascending plankters depends
on the coincidence between the time when the main mass of the population
rises to the surface and the beginning of phytoplankton bloom which, as
was shown above, varies over rather broad limits. Therefore, in early
spring, in some localities we may find older copepodites which have
already risen, but because of food absence, cannot moult and begin
breeding, whereas in neighboring areas, where the bloom has occurred, many
juveniles are already present. Since the regional differences in the

98

time of occurrence of the bloom are determined primarily by the develop-
ment of the summer density stratification of the water it is this factor
which is most important in determining the trophic conditions during the
spawning period.

However, various species do not reach the surface and breed simul-
taneously, but rather in a strictly defined succession. For example,
among the copepods in the Antarctic, the earliest species is C^. acutus,
followed by C^. propinquus, then R^. gigas (Voronina, 1956a). Therefore,
in various places of the area either one or another species is in optimal
conditions and yields the greatest brood. These factors are responsible
for the changes in abundance of each of the species within the limits of
its area of distribution, and the variation in the quantitative relation-
ships between different species. Illustrations of this can be found in
materials from the expeditions of the DISCOVERY (Baker, 1959) and OB'
(Voronina, 1966b).

In some cases, the influence of the hydrologic structure of the
waters is manifested differently. During the spring migration, great
hydrologic gradients may prevent the spawning pool from rising into the
productive layer, and then breeding occurs in the subsurface waters poor
in phytoplankton. This has a sharp influence on the abundance of the
brood (Voronina, 1970a).

These are the main factors determining the regional distribution of
the abundance of new generations of plankters. The distribution is
subsequently transformed under the influence of the currents. The
primary significance is the meridional transfer. The transverse studied
(Deacon, 1937; B. G. Neyman, 1968; Arsen'yev et al . , 1975). The Antarctic
surface water with its population moves northward at a mean speed of
5-20 cm/s (in the Subantarctic, somewhat more slowly). In the zones of
the Antarctic and Subantarctic convergences, the surface waters move
downward, but the organisms remain at their natural depths. As a result,
in these narrow zones there is a continuous increase in the abundance
of zooplankton due to the influx of allochthonous material. The rate of
this increase in one transect through the Antarctic convergence has
been found to amount to 3% per day (Voronina, 1968).

The influence of currents on the distribution of various species
depends on the time spent by their populations in the corresponding
waters. For example, for Euphausia triacantha, which has a two-year
life cycle, inhabiting the surface water and, apparently, performing
only slight seasonal migrations, the peak at the Antarctic convergence
is quite clearly expressed (Baker, 1959), while for the one-year inter-
zonal copepods it is less clearly expressed, although it is still quite
clear. For inhabitants of the middle depths, e.g., Sagitta gazellae, on
the other hand, a great decrease in the population along the convergence
is characteristic, apparently related to the moving apart of their biotope
by the descending surface water. The descending layer has so thoroughly
disjoined these animals that it has facilitated the formation of isolated
populations on either side of the zone of convergence, which have developed
into independent races.

99

The influence of the zone of Antarctic divergence is significantly
weaker, and changes from season to season. In the winter, relatively
rich plankton accumulates here, yielding the maximum spawning pool.
Numerous juveniles appear in spring, moving northward with the surface
water, forming easily visible "spots" (Voronina, 1968). The divergence
influences the distribution of various species differently. Among the
mass copepods, the greatest concentrations are observed for R. gigas, ap-
parently due to the fact that it spends the winter in the higher layers,
where the velocities of the currents are greater than in those inhabited
by C_. acutus and C. propinquus.

Let us sum up our information on zoocenes. Their basic specifics
are: low specialization of the most numerous species: absence of any
attachment to definite depths or water masses, broad feeding spectra;
relationship of periods of breeding and feeding of juveniles to periods
of abundant phytoplankton, as a result of which most species in the
Antarctic are monocyclic, in the Subantarctic, apparently, bicyclic;
significant plasticity of the life cycles; a delay in identical stages
of'cycles in the southern latitudes in comparison to the northern
latitudes; complexity of the picture of quantitative distribution of
individual species, depending on both temporal and local factors.

4.3 Communities.

Specific and trophic structure. The number of species in the pelagic
zone of the Subantarctic, and particularly the Antarctic, waters is
significantly less than in the tropics. Why is this?

The biotopic variety in the temperate and polar waters in the summer,
is no less than in the tropics. There are: surface film, an upper mixed
layer, a residual layer of winter cooling and two thermoclines separating
it from the waters above and below. However, the autumnal mixing disrupts
this stratification, and the time of its vernal restoration is variable.
As a result, ascending populations, at the same time but at different
places, may encounter completely different situations: from complete
homothermy of the surface water mass to well-developed stratification,
from winter shortage of algae to rather abundant bloom. This factor,
apparently, greatly hinders the adaptation of the fauna to the specific
conditions of existence. As a result, neither food specialization of
herbivores, i.e., adaptation to individual stages of succession of phyto-
plankton, nor spatial divergence occurs. As a result of this, the variety
of species in the population is not great. The relationship between low
specific variety of communities and unpredictability of temporal changes
in the environment is well known (Margalef, 1968; Slobodkin, Sanders, 1969).
For the pelagic zone, where the primary consumers of phytoplankton are
located beyond the producing layer for a long time, this factor should
have particularly great significance. Another factor in the low variety of
the population of the higher latitudes may be the brevity of the period
of vegetation of the algae (Heinrich, 1962). In the plankton of the
Southern Ocean, phytophagous forms are clearly dominant, their biomass
in the upper 100 meter layer representing an average of 82%. in places
as much as 96% of the total. The zoophagous animals, the prey of which

100

do not form such abundant concentrations as the phytoplankton , cannot,
under the sharply variable environmental conditions, be very productive.
The absence of the strong pressure of predators, in turn, may help to
maintain the low level of specific variety (Paine, 1966).

All of this shows the great length of the chain of results which
follows from the basic peculiarity of the biotopes of the temperate
and polar latitudes--the seasonal change in solar radiation. First of
all, it assures that the production process is discontinuous, which in
turn defines the basic features of the zoocenes: the character of their
annual cycles, the level of specific variety, their trophic structure.
Therefore, the seasonal changes in solar radiation can be considered
the most important factor determining the peculiarities of cold-water
ecosystems .

The trophic web. The structure of the trophic web of the Southern
Ocean is relatively simple. The phytoplankton is consumed by copepods,
euphausiids and tunicata. All of these are nonselective filter feeders.
The copepods and euphausiids are consumed by the hyperiids, chaetognaths ,
predaceous copepods, squids, fishes and baleen whales. The fishes and
whales also consume amphipods. The fishes and squids are consumed by the
sperm whales and small toothed whales. A definite role in the consumption
of the pelagic fauna is also played by the pinnipedes: the crab-eating
seal feeds almost exclusively on krill, the other seals--on cephalopods
and fishes. Only the Baqridae and sea leopard attack homoiotherms in
the Antarctic.

All of these food chains are of the grazing type. The significance of
detrital chains, which begin with the utilization of dead organic
matter, as well as heterotrophic bacteria in the Antarctic and Subantarctic,
is very low.

This trophic web consists of four main levels: producers, phyto-
phages, and first and second order predators. The baleen whales, fishes
and marine birds, which consume the phytophages and small predators,
occupy an intermediate position between the last two levels. Unfortunately,
this system has no quantitative characteristics, since the production,
and even the biomass, of many groups of organisms, are as yet unknown.
Only approximate data can be presented. The most realistic figures
seem to be as follows. The mean annual biomass of net plankton
(mesoplankton) in the Antarctic in the 0-1000 m layer is 26 mg/m^ (Foxton,
1956), while in the period of the summer maximum, in the upper 100 meter
layer, in the Indian and Pacific Ocean sectors it reaches 10-20 g/m^
(Voronina, 1966b). The greatest mass is that of the copepods (73%), followed
by the chaetognaths (10%) and euphausiids (8%) (Voronina, 1966c). The
biomass of euphausiids, according to trawl data, is about 0.7 g/m^
(Dolzhenkov, 1975), and in regions of their greatest abundance--up to
30 g/m2 (Marr, 1962). The biomass of whales during the period of their
abundance was 0.56 g/m^, their consumption of plankton over the summer
season about 10 g/m2 (Nemoto, 1968; Mackintosh, 1973).

At the present time, a radical restructuring of the quantitative
relationships between individual elements in this web is occurring.

101

As a result of intensive hunting of whales, their initial numbers have
been reduced over the past 40 years by 85-90% (Mackintosh, 1970),
correspondingly decreasing the consumption of their prey. Let us attempt
to discuss the results of these changes on the example of E. superba. We
could hardly expect that the increase in its quantity, estimated as 30
million tons (Mackintosh, 1970), would cause an increase in the
population of its other consumers, since many of them are also intensively
fished. It is more probable to assume that self-regulation of the
population occurs. The increase in the abundance of krill results in an
increase in the intensity of consumption of phytoplankton and a deteriora-
tion in the food supply for the individuals in the population. We can
assume that, as a result of this, a significant portion of the population
will go over, as in the southern waters where food is scarce, to a
four-year cycle. Later maturation will result in a decrease in the
population of the spawning pool.

Since the crustaceans will live longer, they will drift further
north. The zone of their occurrence will expand, but, due to mechanical
factors, will remain within the Antarctic zone. Mackintosh has already
reported unusual northern occurrence of swarms of E. superba (1973).
The transportation of mature crustaceans outside the zone of optimal
conditions for the larvae may also lead to a decrease in the abundance
of this species.

Spatial structure. The pelagic community has a certain spatial
structure, changing regularly with the course of the biologic seasons.
The nature of these changes can be considered on the example of the
three most numerous species of copepods--Calanoides acutus , Calanus
propinquus and Rhincalanus gigas. During the biologic spring, all three
species are present as the overwintered population or, in the case
of the two former species, early juveniles of the new generation. During
this time, the core of the population of C_. acutus is located higher in
the water and its concentration is at its maximum. The core of C^.
propinquus is located more deeply, that of R^. gigas--deeper still. The
spread of the first of these three species may differ, that of the
second is always great. This structure results from the fact that C.
acutus rises to the surface and forms prespawning accumulations earlier
than C_. propinquus , and much earlier than _R. gigas. Later, when the
populations of all three species are in a more advanced state, ^.
propinquus with characteristic domination by egg-bearing females and the
first copepodite stages, for which the surface maximum is typical, takes
up the "feeding" position. At this time, the population of _C. acutus,
in which the second and third copepodites predominate and the fourth
copepodites are beginning to appear, begins to descend into the lower
layers of the epipelagic zone, while R. gigas , which has not yet completed
its spring migration, is still deeper than the other two species. At
the end of the vegetative season, C^. acutus almost completely leaves the
euphotic zone, R. gigas takes up the uppermost position, except in
regions where the sharp seasonal thermocline prevents them from rising.
In the last case C. propinquus occupies the highest position (Voronina,
1972). ~

102

Spring

Fig. ' •-casonal changes in vertical structure of a C' 'ininity. The
diagram ^mo^.s the positions and spread of the core of tne populations of
Calanoides acutus ( 1 ) , Calanus propinquus ( 2 ) , and .Rhincalanus gigas ( 3 )
TVoronina, 1972).

This cycle is illustrated schematically in Fig. 18. This restructuring
of the vertical distribution of plankters during the course of the vege-
tation season occurs at e\/ery point in the water area. It is based on
the changes in the vertical structure of the populations and the asynchronism
of their life cycles described earlier. The earlier occurrence of each
phase of the cycle in the northern latitudes, in comparison to the southern
latitudes^ means that the same sequence of structures will be observed
along a single meridian as we move from south to north.

The maxima of biomass of these species is observed in different
places in space as a result of the asynchronism of the periods of dominance
of the fourth and fifth copepodite stages in the various populations.
(During the period of dominance of these stages the greatest biomass
concentration is achieved.) As a result, the summer maximum of C_. acutus
is always located further south or deeper in the water than that of C^.
propinquus , while that of R. gigas is further north than that of the
other two species (Fig. 19"). A similar divergence of the biomass maxima has
been observed in Subantarctic copepods.

The spatial distribution of locations of maximum concentrations
of various species is also characteristic for chaetognaths (David, 1958,
1965) and euphausiids. Apparently, here also, it is determined by the
asynchronism in the life cycles (Timonin, 1968). In this manner,
competitive interrelationships between similar species are minimized.

The annual cycle in the pelagic zone. The cycles of individual
populations, partially overlapping in time, combine to make up the
seasonal changes in the total quantity of zooplankton. The quantity of
zooplankton in the upper 100 meter layer is characterized (Fig. 20) by
two maxima over the course of the year (Foxton, 1956; Voronina, 1970a, b).
The first, smaller, maximum is related to the spring ascendance of
organisms into the euphotic layer; the second to the development of new

103

fO"

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ZOO -

^^0

:si CfJ 2S! 28 V 2SS 2So 2S7 2S8 2i21yl)

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Fig. 19. Position of maxima of biomass of various species I'f copepods
according to collections from the research vessel OB'. I, Cross section
south of New Zealand, March-April 1956; II, Cross section along gS'^E,
April 1957; III, Cross section from Mirniy to Aden, May 1956; AC,
Antarctic Convergence; 1, Calanoides cutis >25 mg/m^; 2, Calanoides
acutus, >50 mg/m^; 3, Calanus propinquus, >25 mg/m^: 4, Calanus
propinquus, >50 mq/m3; 5, Rhincalanus gigas, >25 mg/m3; 6, Rhincalanus
gigas, >50 mg/m3 (Voronina, 1970) .

generations. The spring migration occurs over a large portion of the
water area in a rather short time, but is delayed in the south. The
summer maximum is observed in the northern zone in February, in the
intermediate and southern 2one--in March. Thus, it occurs in the northern
and middle zone two months later than the maximum of phytoplankton. The
reason for this delay is that the comparatively small overwintered
populations of copepods underutil izes the primary production and does
not prevent the phytoplankton bloom. Only after breeding and growth of
the new generation does effective consumption of algae begin, achieving
a balance that is rapidly followed by overutil ization which, in the
opinion of many researchers, is the main reason for the seasonal drop in
the abundance of phytoplankton. At this time (in April), individual
planktonic animals begin to leave the euphotic zone, causing a decrease
in biomass. In the northern zone, conditions are still favorable for
the vegetation of phytoplankton, and the decrease in consumption leads

104

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105

to a small autumn peak. After the breakup of the seasonal pycnocline,
the winter impoverishment of the epipelagic zone begins.

In the extreme south, the maximum of zooplankton lags behind the
maximum of phytoplankton by only a month. This is not a result of more
rapid development of the zooplankton. The reason is that the early onset
of winter causes earlier descent of plankters from the surface waters.
As a result, some species do not succeed in completing their development
and descend at younger stages.

The difference in time of onset of the maxima for plants and
animals is reflected in their spatial distribution as well. The ring of
phytoplankton bloom is always located further south than the ring of the
summer maximum biomass of zooplankton (Voronina, 1970a, b). In the period
preceding the peak of the zooplankton, the maximum concentrations of
both groups of organisms usually coincide in the upper layer of the
epipelagic zone. Later, they diverge: First, as a result of the over-
utilization of phytoplankton. its absolute maximum shifts deeper than
the maximum of its consumers; at the end of the season, most of the mass
of animals descends into the subsurface layer, while the maximum of algae
remains nearer the surface.

The great amplitude of fluctuations in the population of algae
and the long period of underutil ization of the primary production are
characteristics of the low degree of balance in the cycles of phytoplankton
and zooplankton in the Antarctic. However, the degree of imbalance
apparently experiences significant local fluctuations, depending on the
hydrologic specifics and the composition of the zooplankton. Wherever,
due to a sharp thermocline, the copepods of the winter pool cannot reach
the productive layer (Voronina, 1970a, 1974), primary production is still
more underutilized than elsewhere. The situation is quite different at
the Antarctic Convergence, where the descent of the water decreases
primary production, but the quantity of zooplankton increases due to the
arrival of allochthonic material. As a result, the ratio of biomasses
of phytoplankton and phytophages is significantly lower here than in other
areas and, correspondingly, the degree of its utilization increases. The
maximum balance for the Antarctic is achieved in waters where the plankton
is dominated by euphausiids, particularly E^. superba, which do not perform
seasonal migrations (Voronina, 1970a, b). These large crustaceans, in
the post-larval period, are constantly present in the surface water mass and,
immediately after the beginning of vegetation, can consume the primary
production.

Such is the annual cycle in the Antarctic pelagic zone. The data for
the Subantarctic are too sparse, and can be utilized only for a brief
description. The occurrence of great seasonal fluctuations in the quantity
of phytoplankton indicates that the cycle here is also unstable. However,
the existence of two generations of most phytophages and their rapid
development (thanks to the warmer temperatures) should decrease the period
of underutilization of primary production and result in a greater degree
of balance between the first two trophic levels. These ideas are confirmed
by data on the distribution of bottom sediment in the Southern Ocean.

106

The zone of rich diatomaceous ooze, indicating underutilization of algae
in the pelagic food chains, is bounded on the north by the Antarctic
Convergence and interrupted in the western portion of the Atlantic sector,
in the region of abundance of Euphausia superba (Watkins, 1973).

Thus, the main specifics of the communities of the Southern Ocean can
be characterized by: low species diversity, relatively simple trophic
web; orderly sequencing of the spatial structure, which changes regularly
with time; a long lag between the maxima of phytoplankton and zooplankton
and local differences in the degree of their balance.

107

5, Communities of the Tropical Areas of the Ocean.
(A. K. Heinrich)

The tropical community of the world ocean occupies a tremendous
water area, approximately between 40°N and 40°S. Very significant
faunistic changes occur at its boundaries--transition to the Arcto-boreal
community in the north and the Antarctic community in the south. Many
tropical species extend between these parallels throughout all three
oceans, and some of them are always among the most abundant species.
This creates a structural unity throughout the entire tropical community.
However, it is hierarchical in composition and is divided into communities
in the individual oceans, which in turn are divided into central, equatorial
distant neritic and neritic. Within these, there are other units of
lower rank. Transient communities are found between all of them. The
central, equatorial, distant neritic and neritic communities differ from
each other most strongly. Our task is a description of the structural
and functional peculiarities of the first three types of communities;
neritic communities will be analyzed only for comparison.

The biotopes of the central and equatorial communities are the most
stable parts of the gyres transferring the primary water masses (central
and equatorial), while the biotopes of the distant neritic communities are
associated with less stable gyres of the secondary water masses, arising
as a result of mixing of the primary water masses (C. W. Beklemishev,
1969). The most extensive and unique distant neritic communities are
located in the eastern parts of the oceans, where the eastern equatorial
communities and communities of the eastern boundary currents (California,
Peru, Canary, Benguela) are found, in the locations of upwelling deep
waters. The communities of the currents along the western coasts are
influenced by the influx of water from the temperate latitudes. The
bases of habitats of certain species are maintained by differently
directed currents of surface and deeper layers of water (Longhurst, 1967;
Heinrich, 1974b). The biotopes of the neritic communities are located
in the smaller circulations near the coastlines. The environment here
is much less stable than in the oceanic zones, since it falls under the
influence of the variable wind regimes of the coastal upwel lings of
water and the continental runoff. The boundary, transitional biotopes
arise as a result of mixing of waters and have no closed circulation.
The position of these communities, according to C. W. Beklemishev (1969),
are shown in Fig. 21. The gyres of water maintain the stability of the
physical characteristics and allow the species inhabiting them to remain
in these regions and pass continually through their life cycles.

The peculiarities of the biotopes and related populations are
created by the climate. The peculiarities of the various water masses

108

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109

forming the biotopes are related to the physical conditions in which
they were formed. Therefore, these biotopes are distinguished by the
thermohaline characteristics of the waters, the vertical distribution of
water density, the predominant directions of vertical water movement,
the transparency of the water, the annual mixing cycles, the quantity
and composition of nutrients and many other properties which influence
productivity and--directly or indirectly--the composition of the population
(C. W. Beklemishev, 1969; Bogorov et al . , 1958; Koblentz-Mishke et al . ,
1970: Semina, 1974).

5,1 Structure of Tropical Communities

Peculiarities of species composition and boundaries between communi-
ties. Significance of expatriated species. The tropical oceanic communi-
ties include a significant number of widespread species. In the oceanic
communities of the Pacific Ocean, among the euphausiids, chaetognaths
and foraminifers, taken together, widespread tropical species amount
to some 50% of the total number (Heinrich, 1975a). In all communities
there are also groups of more narrowly distributed species, which have
bases of habitats in one or two large-scale gyres only. These are
specific species for the communities. Within the communities of the cen-
tral waters, these include the central (southern, northern and bicentral)
species, in the equatorial communities--equatorial species, in the
distant neritic communities--transient, peripheral and distant neritic
species (C. W. Beklemishev, 1959). Among the euphausiids, chaetognaths and
foraminifers, these species represent 19% of those found in the north
central community of the Pacific Ocean, 16% of those found in the equa-
torial community.

Specific species may be absent around the edge of a gyre, so that
all species are encountered only in a certain portion of the area.
As a result of this, some heterogeneity develops in the composition of
the population, even within a single gyre. Furthermore, organisms are
transferred from one gyre to another with turbulence and individual
streams of water. Turbulent mixing allows plankton to be carried even
against the constant current (C. W. Beklemishev, 1959). Many species have
broad areas of expatriation. The areas of expatriation of species with
various types of ranges cover significant portions of the central and
equatorial communities. Due to this, when communities are crossed in the
meridional direction, the appearance of certain species and disappearance
of others is a normal phenomenon, and the boundaries of the community are
not clearly defined (Heinrich, 1975a, b).

Nevertheless, as the use of methods of numerical taxonomy has shown,
the differences between the communities are quite genuine, and the zones
with the most homogeneous population are generally located within the
boundaries shown in Fig. 21 (Heinrich, 1977).

The expatriated species create dependent lower-rank communities
within the equatorial and central communities. Their existence results
from the influx of water from neighboring communities. Into the equatorial
communities central species penetrate from both central communities
and the distant neritic species, while into the central communities

110

penetrate equatorial species, peripheral, transient and distant neritic
species. The expatriated species have considerable significance in the
structure of the communities. In terms of the number of species as a
whole for the euphausiids, chaetognaths and foramini fers , in the north
central community of the Pacific Ocean, their number is about as great
as the number of specific species, and in the equatorial community, they
are even 50% more numerous. This indicates the interdependence of
neighbouring tropical communities (Heinrich, 1975a).

In tropical ocean communities, the greatest numbers are, as a rule,
achieved by the wide-spread tropical species and specific species.
Expatriated species are not numerous.

Changes in the number of widespread species. Some questions
arise: Just what is the large-scale pattern of distribution of the
number of widespread tropical species? Is it similar in different
species? Is there similarity between the distribution of areas of
abundance of widespread tropical species and ranges of species with
relatively narrower areas of distribution, equatorial, central, and
distant neritic species? What are the small-scale changes in populations
of wide-spread tropical species, and what factors cause them?

Work in the Pacific and Indian Oceans on the distribution of the
chaetognaths, euphausiids, copepods, Siphonofora, mollusks (Bieri, 1959;
Brinton, 1962; Heinrich, 1960, 1968; Vinogradov, Voronina, 1962, 1963;
Chiba, Hirakawa, 1972; Musaeva, 1973; Gueredrat, 1974; Sakthivel, 1973)
have shown that the abundance of the widespread tropical species changes
significantly from one region to another, and that their distribution
is different. If we analyze the large-scale patterns of distribution of
population, we can distinguish four main types of distribution: 1) maxi-
mum abundance in equatorial waters; 2) maximum abundance in central
waters; 3) difference between abundance in equatorial and central regions
slight or zero; 4) maximum abundance in one of the distant neritic regions

Each type has variants, and there are transitions between types.
Each type of distribution includes species of all trophic levels. The
basic large-scale regularities of horizontal distribution of abundance
of animals are retained throughout all seasons, and from year to year
(Heinrich, 1968. 1973; Chiba, Hirakawa, 1972; Gueredrat, 1974).

The large-scale pattern of distribution of species of various
types can be reduced to the statement that areas of great abundance of
some widespread tropical species are located approximately within the
regions inhabited by most of the central species, of others--where most
of the equatorial oceanic or distant neritic species live. In neighboring
regions, over great areas the abundance is small, though there are some
small, apparently unstable, spots of higher density.

In the western Pacific, areas have been distinguished for copepoda
with each type of distribution, in which most of these species have
maximal abundance. These areas diverge spatially quite clearly for the
species with the maximum abundance in the equatorial and central regions,

111

and the boundaries between them practically coincide with the boundaries
of the equatorial biogeographic province of C. W. Beklemishev (Heinrich,
1968). Each boundary of the equatorial province is the midline between
two boundaries, one of which separates the 50°/ core of the equatorial
species, the other the corresponding core of the central species (C. W.
Beklemishev, 1969). Consequently, the equatorial, central and distant
neritic communities, in addition to the specific species which are
theirs alone, are also distinguished by the set of species which reach
maximum abundance there.

The existence of groups of species with different types of large-
scale changes in abundance is directly or indirectly (through biologic
interrelationships) related to the peculiarities of the biotopes of the
central, equatorial and distant neritic communities. The combination of
these peculiarities is determined by the hydrologic and hydrochemical
environments and productivity. It is possible that their combined
influence is significant (Fager, McGowan, 1963).

The increase in the abundance of certain species around the periphery
of the tropical area apparently results from a decrease in competition,
since many tropical species disappear here, and the number of some others
decreases (Tokioka, 1959; Voronina, 1962: Heinrich, 1964, 1968; C. W.
Beklemishev, 1967).

Relatively small-scale changes in the abundance of species occur
within individual communities. In the equatorial communities of the
Pacific and Indian Oceans, the position of the band of high abundance
of various species is related to the position of divergences and con-
vergences. Transport by currents is also important, as a result of which
the bands and spots of high abundance of species, developing one after
another in time, also diverge in space (Vinogradov, Voronina, 1962. 1963).
Within the northern central community in the western Pacific, the dis-
tribution of the maximum abundance of wide-spread tropical species of
copepoda of the second and third types of distribution has been found
to be connected with the areas of greater productivity located around the
halistasis. In the center of the halistasis, where the biomass of zoo-
plankton was minimal (less than 3 g/m2 in the 0-500 m layer), none of
these species produced spots of high abundance (Heinrich. 1968).

Number of species and dominance. The tropical oceanic communities
are richest in numbers of species. The number of species varies within
the tropical communities. In the tropical regions of the Pacific Ocean,
the number of species of euphausiids, chaetognaths and foraminifers
changes, when we consider the impoverished peripheral regions, by a
factor of 2-3, or if we ignore the periphery, by a factor of 1.5-2
(Heinrich, 1974a). In various taxonomic groups of animals, the changes
occur differently. The outlines of regions with the greatest number of
species recall the outlines of the ranges of planktonic animals, since
in each such group, species predominate with certain types of distribution,
However, these regions agree rather well with the boundaries of the
equatorial, central and distant neritic communities. Thus, for the
chaetognaths, the greatest number of species in the distant neritic

112

a

communities is characteristic. The foraminifer fauna in the Pacific
Ocean is richest in the equatorial community, while the greatest number
of species of euphausiids is observed in the central community. The
Siphonofora in the Atlantic (Margulis, 1972, 1974) and Indian (Musaeva,

1973) Oceans, as well as the salps in the Atlantic Ocean (Kashkina,

1974) have the greatest number of species in the equatorial and distant
neritic communities, rather than in the central communities. The increase
in the number of species in communities of a certain type is preserved
at least for the chaetognaths in all three oceans.

In the transient communities between the high-latitude and tropical
communities, the number of species in all groups is low, in spite of the
simultaneous presence of species of different origins, a result of the
gradual impoverishment of the fauna toward the periphery of the tropical
community. Within the tropical community, the faunistically richest
areas are also located in the central, equatorial and distant
neritic communities, not in the transient zones between them. The
transient biotopes are not favorable for many species from the neighboring
communities; therefore, the mixing does not produce enrichment of the faun._
in these zones. In the neritic regions, the number of species of planktonic
animals is less than in the oceanic ones (Heinrich, 1952; Bowman, 1971).

The tropical oceanic plankton is distinguished by a relatively low
dominance of individual species. The dominance varies from season to
season and from region to region. In the Indian Ocean, the dominance
among copepods increases from regions with stable water stratification
or with feebly marking water sinking toward regions with upwelling of
water, while species diversity of filtering copepods (based on biomass
using the formula of Shannon), conversely, decreases (Timonin, 1969,
1972). Thus, in zones of upwelling of water, 75?. of the biomass of
Calanoida is accounted for by three species, while outside the upwelling
zones, the five or six most numerous species make up only 30-40?. of the
biomass. A similar picture is observed for the chaetognaths and euphausiids,
In the equatorial area of the Pacific Ocean, the intensity of upwelling
of water decreases from east to west, and the standing stock of plankton
decreases, while the species diversity of large copepods and euphausiids
simultaneously increases (Gueredrat et al., 1972), and still greater
species diversity of euphausiids is observed in the south central community
(Roger, 1974).

Thus, in equatorial communities, where upwelling of water is stronger
and more frequent, we can expect a greater dominance of individual
species than in the central communities.

In the distant neritic communities in currents along the western
coasts of the continents, and in neritic communities, dominance of one
or two species is quite clear. In the region of the California Current,
an increase has been shown in the dominance of the two most numerous
species in the direction from the ocean to the shore, and the species
diversity of zooplankton decreases to the shore, as evaluated by the
Fisher coefficient (Longhurst, 1967).

Taxonomic and trophic groups. In the tropical oceanic communities,
in comparison to the Arcto-boreal communities, the relative quantity of

113

Gymnoplea decreases, while Podoplea, Ostracoda, Tunicata, Polychaeta,
Coelenterata and Chaetognatha increase. Thus, due to the greater relative
quantity of Polychaeta, Chaetognatha and Coelenterata, the significance
of predators increases. Furthermore, there are many more predators
among the Gymnoplea (Heinrich, 1951b, 1968; Timonin, 1969, 1973; Bsharah,
1957; Deevey, 1971; Grice, Hart, 1962; Gordeeva, Shmeleva, 1971; Greze,
1971).

In tropical plankton, in contrast to boreal plankton, a single
function in the food chain is distributed more evenly among various
taxonomic groups. One good example of the composition of tropical
plankton is its composition in the western Pacific in the section along
174°W between 30°N and 30°S. The copepods average about half of the
biomass of zooplankton, 2/3 of them being Gymnoplea. About 20% of the
biomass is accounted for by the Ostracoda, about the same amount by the
Chaetognatha, 10°^ by the Coelenterata and Polychaeta, while the Tunicata
account for a small amount.

Changes in the number, size and, therefore, biomass of the various
groups are found along the meridian (Heinrich, 1968). The quantities of
many animals (Radiolaria, Foraminifera, Coelenterata, Copepoda, Gastropoda,
Chaetognatha) more or less regularly increase in the equitorial region,
but the Ostracoda, Amphipoda and Salpidae, conversely, are more abundant
in the central regions. In the equatorial region, the biomass of Copepoda
amounts to 55-75%, in the central regions--35-50% of the total biomass
of zooplankton, the relative quantity of Ostracoda increasing from 10%
in the equatorial region to approximately 20% in the central regions. The
share of the Salpidae in the total biomass increases toward the periphery
of the tropical area.

In the Indian Ocean, primarily within the eutrophic equatorial
community, the composition of plankton depends on water regime (Timonin,
1969, 1973). In regions with upwelling of water, Gymnoplea account for
70% of the biomass, in regions with stable water stratification--only 40%.
The Chaetognatha are relatively scarce (less than 10%) under conditions
of upwelling of water, more numerous (12-27%) under stable stratification
or with weaker upwelling of the water. The details of the trophic
structure also change. In regions of intensive upwelling of water with
high biomass of zooplankton and relatively large numbers of Copepoda,
filter feeders predominate (over 50% of the total biomass of zooplankton),
among these about 90% being coarse filter feeders. Seizing and swallowing
predators make up 20-25% of the total. With weak upwelling of water, the
filter feeders are fewer (40%), and half of them are fine filter feeders.
Seizing and swallowing predators amount to 30-35% of the total. When there
is no upwelling of water, with low zooplankton biomass, filter feeders
represent still less (20-30%), while the number of seizing and swallowing
predators increases to 45%.

Similar results were obtained in the Bay of Guinea in a study of the
relationship of trophic groups among Copepoda in various seasons (Samyshev,
1973) and in the Sargasso Sea, where, during a short period of upwelling
of water, a sharp peak was observed in the abundance of the coarse
filter feeder Eucalanus hyalinus, while throughout the rest of the year,
various species of fine filter feeders predominate (Deevey, 1971; Grice,
Hart, 1962).

114

The zonal changes in the composition of the tropical zooplankton are
related to these regularities. Although in equatorial communities, areas
may be found without upwelling of water, on the whole upwellinq pre-
dominates in these communities. Therefore, in the Pacific Ocean, within
the equatorial region, an increase was observed in comparison with the
central regions in the relative quantity of Gymnoplea.

In the Indian Ocean, areas with predominance of filter feeders are
also found within the equatorial community. The central regions are
characterized by stable water stratification or water sinking, upwelling
being rare and weakly expressed. Therefore, within the central community
of the Indian Ocean, between 20 and 29°S, A. G. Timonin found small
quantities of herbivorous filter feeders and relatively larger quantities
of predators in all locations.

In the Pacific Ocean on the equator between 95 and 160°W, a population
which did not fit into this system was found (Vinogradov, Semenova, 1975;
Flint, 1975). In spite of clear upwelling of water and abundant plankton,
the upper 200 m was dominated by predators, which composed about 60% of
the biomass. Toward the west, as the upwellinq of water weakened and
the biomass of plankton decreased, the relationship of the trophic groups
remained essentially the same. As yet, no satisfactory explanation for
this has been found, but this composition of the population is not typical
for the broad oceanic tropical regions.

Around the peripheries of the tropical area, the relative quantities
of Tunicata increase, particularly the Salpidae and Pyrosoma (Heinrich.
1964, 1968). These are filter feeders with a broad diet. This regularity
is seen in all oceans. An increase in the quantity of Salpidae has also
been noted in certain inshore regions in the lower latitudes and in zones
of upwelling of water (Yount, 1958; Russell, Colman, 1935; Rao et al . ,
1973; Gordeeva, Shmeleva, 1971; Gruzov, 1971). There are insufficient
data for comparison but, apparently, at least in the open ocean, these
swarms are less frequent and not as great as in the peripheral tropical
areas.

In the distant neritic communities of the eastern boundary currents
the relative quantity of Copepoda is great, clearly dominated by the
coarse filter feeders, both herbivores and omnivores, while predators
are few. For example, in the Peru Current, according to M. E. Vinogradov
and T, N. Semenova (1975), predators represent less than 10% of the
biomass. In the Benguela Current, the large herbivorous and omnivorous
Copepoda represent 80-95% of the biomass (Andronov, 1971). In the
California Current, in a region of upwelling water, predominance of
coarse herbivorous filter feeders (Copepoda and Decapoda Pleuroncodes
planipes) is also seen. With increasing distance from the coast, toward
the central waters, the relative number of predators increases (Longhurst,
1967).

The zooplankton of neritic communities is usually dominated by the
Copepoda. These are most frequently small Copepoda, herbivores or
omnivores. One significant feature of the trophic structure of many

115

tropical neritic communities, particularly in regions with strong upwelling
water, is the presence of common commercial fish, feeding on the phyto-
plankton (Heinrich, 1970; Rojas de Mendiola, 1969). Off the coast of
California, both in the distant neritic and in the neritic region, the
most important herbivore is the pelagic stage of the Decapoda Pleuroncodes
planipes (Longhurst, 1967). In the oceanic regions, there are no
herbivorous fish, and the food chains are long (Heinrich, 1962; Parin,
1968).

5.2 Production Cycles

The production cycles of communities are seen here as the relation-
ship between the seasonal cycles of the phytoplankton and mesozooplankton
and, as possibly, the higher trophic levels. Yu. I. Sorokin (see IV. 2)
assigns an extremely important role to bacteria, although his conclusions
are not universally accepted (Steemann Nielsen, 1972; Banse, 1974;
Skopintsev, 1972). Due to the lack of year-round observations of
bacteria and protozoa in the open ocean, their participation in the
production cycle will not be discussed in this book.

Two extreme types of production cycles are theoretically possible:
balanced and unbalanced (Cushing, 1959a). In a balanced cycle, throughout
the year the daily grazing of live algae is equal to their net production.
Regulation is achieved through the relation of production and consumption
of algae, the rate of breeding and growth of herbivores and regeneration
of nutrients with an extremely short delay period between the beginning
of an increase in the quantity of algae and an increase in their con-
sumption. Similar dependencies occur at the higher trophic levels as
well, but the regulation of trophic relationships in nekton animals occurs
not so much through breeding as through migration. Stability of abiotic
conditions helps to maintain this type of cycle. In contrast to this,
with an unbalanced production cycle, the production of algae fluctuates
widely due to the effect of unstable abiotic conditions, herbivores
develop slowly. There is a long delay period, during which grazing
increases to match the increased production of algae; in some cases,
this occurs only after the algae reach their maximum quantity which is
possible given the reserve of nutrients available. The algae are under-
utilized for a long period of time. Cushing considered that these cycles
do not exist in nature in clear form, but that the tropical communities
located outside the regions of strong upwelling of water are closest to
the balanced cycles, while the cycles of communities in the temperate
and polar waters are closest to the unbalanced cycles.

Factors in the seasonal development of plankton. The physical
factors which create instability in the production cycles of tropical
communities are primarily those which facilitate the seasonal develop-
ment of phytoplankton.

In the high-latitude edges of central communities, they are close
to those in the boreal area. Thus, in the Sargasso Sea (see Fig. 21),
the peak of phytoplankton is formed in the spring, soon after stability

116

is established in the water after the winter mixing, caused by cooling
and, possibly, by the winds. In the winter, there are small, short,
sporadic pulses of phytoplankton, depending on the weather, since, in
contrast to boreal waters, the intensity of light in the winter is not
so low as to prevent development of algae. In the summer, thermal
stratification is established and phytoplankton is scarce. Its production
depends on the recycling of nutrients and random mixing of the water
during storms (Riley, 1957; Menzel , Ryther, 1960).

Apparently, in other oceans as well around the periphery of the
tropical area the winter cooling is of great significance for the mixing
of water, enrichment of the surface layers of the water with nutrients and
subsequent development of plankton. For example, in the Pacific Ocean
in the region of 40-26°N along 155°W, the winter development of phyto-
plankton is explained by the deepening of the thermocline due to cooling,
as a result of which the nutrients reach the euphotic zone, where they
are immediately utilized by the phytoplankton, so that the increase in
their quantity is almost unnoticeable (McGowan, Williams, 1973).

In the southern Indian Ocean, to the west of Australia (see Fig. 21),
in the region of 18-32°S, the decrease in the quantity of phytoplankton
at the end of southern hemisphere summer results from thermal stratifi-
cation. The increase in the quantity of phytoplankton in the winter
corresponds to the breakdown of this stratification. The quantity of
nutrients changes very little from season to season, which is also
apparently related to the immediate consumption of nutrient salts by the
algae (Tranter, 1973).

In the lower latitude tropical regions, winter cooling does not
occur, thermal stratification is well developed for a long period of
time, and the most important factor in the seasonal development of the
plankton is the wind. The winds cause mixing of the water or shifting
of currents and the related upwelling of water.

In the eastern Indian Ocean (see Fig. 21), between 9 and 18°S, the
increase in the quantity of phytoplankton and zooplankton in the winter
is related to the upwelling of water in the southern equatorial current
caused by the monsoon (Tranter, 1973). This region belongs to a distant
neritic community, but even within the equatorial community of the
Indian Ocean, the succession of monsoons has a significant influence on
the course of development of plankton (Kabanova, 1968).

In the equatorial community of the Pacific Ocean in the region
between 120°W and 180°W from 5°S to 10°N, the maximum of seston is
noted in April-June in the Equatorial Countercurrent, and in October-
December in the South Equatorial Current, which coincides with the
reinforcement of the trade winds (King, Hida, 1957). The periodicity of
seasonal changes in the quantity of plankton in the distant neritic
community of the currents along the western coasts of the continents is
related to the upwelling of water as has been shown, e.g., for the
region of the California Current. The upwelling of water itself depends
on the wind regime (Walsh et al . , 1974).

117

In the neritic regions, the factors in the seasonal development of
phytoplankton include everything which facilitates enrichment of the
euphotic zone with nutrients (Heinrich, 1961a, b; Sournia, 1969;
Khromov, 1973). Nutrients arrive either from the deeper layers of water
or from the land. Therefore, the wind regime mixing the water, driving
it away and thereby facilitating upwelling of water, and the regime of
precipitation, bringing mineral salts from the land, are both important.
However, the seasonal changes in phytoplankton are not the same in all
the neritic tropical regions. Local peculiarities change the climatic
effects so strongly that even in closely located sections, the seasonal
Cycle of development of phytoplankton may be quite different (Sournia,
1969; Motoda, Marumo, 1963). In particular, this cycle is influenced
by the degree of unevenness of the shoreline, the proximity of estuaries,
etc. The earlier assumed (Bogorov, 1941) monocyclic development of
phytoplankton in the tropical drea, with a winter peak, may be character-
istic only of the marginal high-latitude regions.

Peculiarities of production cycles in the main types of tropical
communities. Rather complete studies of production cycles of oceanic
communities, with observations over the course of a year or more, have
been conducted in the regions shown in Fig. 21. The section in the
Indian Ocean is located in a distant neritic region, but the composition
of the zooplankton during the period of the survey was typical for oceanic
regions. Apparently, the course of seasonal phenomena in the southern
portion of the section is characteristic for the central community,
while in the northern portion it is close to that of an equatorial community,
The survey in the Pacific Ocean combines equatorial oceanic and distant
neritic sections, which probably differ little from each other in their
seasonal cycles far from the coast. Unfortunately, materials have been
collected and processed in different regions by different methods and,
except for the stations in the Sargasso Sea and the section in the Indian
Ocean, the intervals between subsequent observations are longer than a
month. In the Guinea Bay, the annual cycle of plankton has been composed,
based on data for several years, with observations in any given year
lasting only two or three months.

The similarity of a production cycle to any given type can be
determined directly by comparing the rates of production and consumption
over the course of a year, or indirectly, by keeping in mind the amplitudes
of fluctuation of biomass of the various trophic levels, the duration of
the delay of consumption, the ratio between the biomass of food organisms
and the organisms which feed upon them. Both methods yield only approxi-
mate descriptions of a cycle.

The production cycles of oceanic tropical communities are more nearly
balanced than the others. For example, in the Sargasso Sea, the Indian
Ocean (cross section along 110°E) and in the Central Pacific, the
quantity of nutrients, phytoplankton and zooplankton is low and stable
throughout the year (Steemann Nielsen, 1958; Gushing, 1959a, b; Menzel ,
Ryther, 1961; Tranter, 1973; King, Hida, 1957; Blackburn et al . , 1970).

118

The ratio of the quantity of phytoplankton to the quantity of
zooplankton is low. In the Indian Ocean in the 0-200 m layer with
observations made once per 2 months it fluctuated, based on the content
of C, between 1.4 and 6 (Tranter, 1973). In Guinea Bay, in the 0-100 m
layer, with observations made once per month, the ratio of phytoplankton
to zooplankton, based on wet weight, was 0.05-0.5 (Gruzov, 1971). In
the North Atlantic and Polar basin, the ratio of wet weights of phyto-
plankton and zooplankton is 10-100 in the spring, 1-5 in the summer
and less than 1 only in the winter (Bogorov, 1938).

All of this indicates the greater degree of utilization of phyto-
plankton by zooplankton in the tropical community. According to Steemann
Nielsen (1958), the seasonal stability of the quantity of algae and
significant homogeneity of their distribution in space, characteristic
for oligotrophic tropical regions, can be achieved only as a result of
grazing by herbivores. If grazing did not limit growth, the fluctuations,
as observed in cultures, would be significant, and at the moment of
utilization of the reserves of nutrients, the growth of algae would stop
completely, which is not observed in oligotrophic regions. Certain
experimental observations confirm this phenomenon as well. In the
Sargasso Sea, after relatively large particles (presumably consumers)
are removed from the water, the quantity of small particles, primarily
algae, increases (Sheldon et al . , 1973). In the central waters of the
North Pacific, primary production in the euphotic layer agrees simultane-
ously with the rate of arrival of nutrients from the deeper layers and
the rate of excretion of zooplankton (Eppley et al . , 1973).

A near balanced production cycle is reached in these regions
primarily due to the relatively stable abiotic factors. A second important
factor is the short delay period of grazing. For most planktonic Copepoda,
breeding continues throughout the year (Gueredrat, 1974; Woodmansee,
1958; Farran, 1949), one generation following another, with no clear
domination of any given stage of development. Therefore, as the quantity
of phytoplankton increases, the quantity of herbivores can increase
rapidly by the growth of already existing juvenile and middle stages and
by breeding and subsequent development of a new generation. As the
quantity of phytoplankton increases, the breeding rate of the Copepoda
increases (Prasad, Kartha, 1959). Judging from observations in inshore
regions, generations of tropical Copepoda are short when food is
abundant. Off the coast of India, a generation of Acartia erythraea
develops in a week (Subbaraju, 1967). The development of a generation
of Paracalanus crassirostris in culture requires a minimum of 2 weeks
(Lawson, Grice, 1973) . Under oceanic conditions, we can expect longer
generations, particularly after long periods of starvation, but still,
year-round breeding and the varied age composition should help to reduce
the delay period.

The structure of oceanic communities, characterized by a diverse
species composition, the lack of strong dominance of a few species and
a complex, branched food net with many trophic levels can also facilitate
a stable production cycle.

119

Significant differences in the interrelationships of phytoplankton
and zooplankton can be found between the equatorial and central com-
munities in the Pacific and Indian Oceans. For example, in the equatorial
region of the Pacific Ocean (at 174°W), the ratio of the quantity of
phytoplankton to zooplankton is higher than in the central regions. In
the equatorial region there is a significant and high correlation between
the biomass of phytoplankton in the 0-100 m layer and the biomass of
zooplankton in the 0-500 m layer (r = 0.84; P = 0.95), while in the central
regions this correlation is low and insignificant (r = 0.08; P < 0.95)*.

In the Indian Ocean, within the equatorial distant neritic community,
significant positive correlation has been noted (Tranter, 1973) between
zooplankton and primary production, zooplankton and nutrients, which is
explained by the high value of immediate regeneration of nutrients through
the excretions of the animals. In the "subtropical zone" of Tranter,
corresponding to our central community, a positive correlation was noted
only between phytoplankton and primary production, which determined their
direct functional relation, in spite of the weak influence of other effects.

It was found that in the equatorial community of the Indian Ocean,
the delay in the development of zooplankton and its grazing of phytoplankton
was shorter than in the central community. In the equatorial region,
there is no significant correlation between the quantity of phytoplankton
and zooplankton upon simultaneous observation. When phytoplankton is
compared with zooplankton collected at the same station after one or two
weeks, the correlation coefficient becomes higher and significant. When
phytoplankton is compared with zooplankton collected after 6-8 weeks, the
correlation coefficient decreases once again. In the central community, a
comparison of simultaneous collections and collections with intervals of
3-4 weeks reveals a correlation coefficient which is either positive,
but low and statistically insignificant, or negative, but comparison of
samples collected with a delay of 6-8 weeks yields a higher positive,
significant correlation between phytoplankton and zooplankton.

The reason for the long delay period in the central community is
the less constant enrichment of the surface waters with nutrients, the
greater duration of the period of low productivity, during which the
herbivores starve, and the greater grazing of herbivores by predatory
micronekton, the population of which is supplemented by drift from the
north (Tranter, 1973). The long delay retards the remineral ization
of nutrients and increases the imbalance. The decrease in the rate of
development of animals under conditions of starvation has been proven,
at least for neritic Copepoda (Woodmansee, 1958; Ummerkutty, 1967).

*The decimal logarithms of biomass of phytoplankton and zooplankton
were used to calculate the correlation coefficient. The biomass of zoo-
plankton was calculated on the basis of the number and individual weight of
the animals (Heinrich, 1961a), the biomass of phytoplankton was taken
from G. I. Semina).

120

During the course of the year, the relationships between phytoplankton
and zooplankton change. It is impossible to estimate the length of the
periods of overutilization and underutilization by the methods now used.
The small fluctuations in phytoplankton and its small quantities during
the peak period indicate that there is not a long period of underutilization.
Overutilization is possible, but since the mean annual balance is obviously
not negative, a status near the balanced state is probably predominant.

In the Indian Ocean, the production cycle in the lower levels of the
food chain is apparently better balanced in the equatorial community than
in the central community. Due to the shorter delay in the equatorial
community, brief periods of underutilization of the phytoplankton are more
rapidly eliminated. The high correlations of simultaneously studied
zooplankton, nutrients and primary production show that the zooplankton
plays the primary role in regeneration of the nutrients. In the central
community, the delay in grazing of phytoplankton is longer, and there is
no close correlation between zooplankton and the regeneration of nutrients.

In both parts of the section, Tranter also found anomalous, hard-to-
explain relations between trophic levels which, in his opinion, resulted
from mixing of waters of different origins, thus disrupting the balance.

Attempts at direct estimation of the degree of balance of production
of phytoplankton and its consumption by zooplankton over the course of an
annual cycle were undertaken in the Sargasso Sea (Menzel , Ryther, 1961)
and the Guinea Bay (Gruzov, 1971, 1973). In the Sargasso Sea, the daily
needs for the metabolism of all zooplankton in the 0-500 m layer was
found to be close to the daily primary production throughout the entire
period of observation (2.5 years). If we consider the needs for the
growth of animals (which was not done), the total consumption of algae would
be still higher. In the opinion of the authors, in the Sargasso Sea the
cycles of algae production and herbivore grazing are balanced, and
practically all of the production of algae is eaten. The comparisons of
Menzel and Ryther (1961) were based on approximate calculation; further-
more, it was not taken into consideration that some of the animals are
predators. The peaks in the curves did not coincide precisely, there were
delays of 2-4 weeks in the zooplankton, and some of the small peaks in
primary production were not accompanied by peaks on the curve of zooplank-
ton respiration.

L. N. Gruzov (1971, 1973) determined the daily consumption of
zooplankton in Guinea Bay, based on the needs for respiration and growth
of the animals. It was found that over most of the year the trophic
relationships of algae and herbivores were balanced, with underutilization
occurring only immediately after the upwelling of the water in June. The
large generations of herbivores then formed restored the balanced state.
It was not stable, and was replaced by overutilization, which was replaced,
in turn, by balance with low primary production and a small number of
herbivores. A large number of assumptions were made in the calculations;
therefore, their accuracy is low, and we cannot say how long the state of
balance was retained during the year. However, there were doubtless
fluctuations, and the directions of the deviations were probably properly

121

estimated. A more precise estimate of the degree of balance is probably
impossible at present.

The annual cycles in the relationships of herbivores and predators
in the tropical ocean regions are not nearly so well known. The micro-
nekton, including the animals caught by an Isaacs-Kidd trawl, in the
equatorial region of the Indian Ocean produce an annual maximum of
biomass after the maximum of mesoplankton. The highest correlation
coefficient between zooplankton and micronekton, i.e., small fishes and
squids, is obtained by comparison of samples collected at intervals of
6-12 weeks (Legand, 1969; Tranter, 1973). This is explained by the
longer development of the larger animals. However, in the central region,
and in some seasons also in the equatorial region, no such regularity is
observed. It is assumed that under these conditions the zooplankton
and micronekton are related to the mixing of waters of different origins.
The quantity of micronekton in these regions is more stable than the
quantity of zooplankton or the value of primary production. Here,
advection increases the stability in the interrelationships of the higher
levels of the trophic chain (Tranter, 1973).

In the eastern Pacific (see Fig. 21), the amplitude of seasonal
fluctuations of fishes and squids is similar to that observed for algae
and zooplankton, but the maximum of their biomass occurs during the
period of the minimum of zooplankton, meaning that there is a delay of
four months when observations are made once each two months. The seasonal
changes of biomass of micronektonic crustaceans are statistically sig-
nificant only at the Equator; their maximum coincides with the maxima
of phytoplankton and zooplankton (Blackburn et al . , 1970).

Thus, due to the longer period of development of micronekton, its
increase in quantity lags behind the increase in quantity of zooplankton
by 1.5-3 months, which introduces elements of instability to the balance
of production and consumption. Sometimes, the quantities equalize at
various times in the year due to advection, while in other cases advection,
probably, may lead to the opposite result. The amplitudes of fluctuations
of the quantity of micronektonic fishes and sauids are not great. In the
eastern Pacific, their quantity during the maximum is approximately
double that observed during the minimum, and their seasonal variability
in both communities of the Indian Ocean is still less (Blackburn et al . ,
1970; Tranter, 1973). The fluctuations in the quantity of micronektonic
crustaceans in the eastern Pacific are quite small, with the exception of
the Equator, where the maximum is 15 times greater than the minimum
(Blackburn et al , , 1970). This has not as yet been explained. As we noted
earlier, this region is also distinguished by a unique composition of
plankton.

Large nektonic animals (tuna, whales) in the Indian Ocean migrate to
the areas of seasonal concentration of micronekton, with which they are
connected primarily through the squids and certain fishes, immediately
before its maximum (Tranter, 1973). This increases the stability of the
trophic relationships.

122

w

In many tropical neritic communities, in contrast to the oceanic
communities, the trophic relationships of phytoplankton and herbivores
are essentially unbalanced (Heinrich, 1970) for long periods of time.
The phytoplankton is abundant and underutilized. The fluctuations in
quantity of phytoplankton are great. Along the west coast of India, e.g.,
the number of algae during the maximum exceeds their number during the
minimum by a factor of 150 (Subrahmanyan, 1959), and the maximum mean
monthly biomass of algae in the Gulf of Panama is 57 times greater than
the minimum one (Smayda, 1966). The ratio of the quantity of phytoplankton
to the quantity of zooplankton in the Gulf of Panama varies from 0.04 to
980, averaging 83, and at times reaches ratio characteristics for boreal
communities (Smayda, 1956). Based on the calculations of this author,
the daily rate of grazing of phytoplankton by herbivores is only 20-44% of
the daily primary production.

The weak balance of trophic relationships in neritic tropical
communities in comparison to oceanic communities is explained first of
all by the instability of environmental conditions, the strong but
inconstant enrichment with nutrients as a result of upwelling of water
and runoff from the land. In places where, as at the Great Barrier Reef,
the mixing regime is constant, and there is no runoff from the land, the
quantity of phytoplankton is low and its fluctuations are slight throughout
the year (S. M. Marshall, 1933). Furthermore, neritic communities have
a simpler structure than oceanic communities (smaller number of species,
with relatively strong dominance of a few species, predominance of short
food chains). This reduces the possibilities of regulation of trophic
relationships of the organisms and thereby facilitates instability in
the production cycle.

The distant neritic communities in the eastern boundary currents
are, like the neighboring neritic communities, under the influence of
strong upwelling of variable intensity. Some of the nutrients and
phytoplankton may reach there due to advection from neighboring neritic
regions. These regions are dominated by large herbivorous Copepoda, while
herbivorous fishes are not of essential significance. In the California
Current, Pleuroncodes planipes is abundant both in the neritic and in
the distant neritic region (Blackburn, 1959). Changes in the intensity
of upwelling of water during the course of the year lead to alternation
of oligotrophic and eutrophic periods and changes in the trophic relation-
ships in the community (Gushing, 1971). For example, in the Peru Current
in September-November, phytoplankton is consumed in the regions off the
shelf quite intensively, while in June there is much less zooplankton,
and the consumption of phytoplankton has been estimated to be less than
10% of its daily production (Beers et al . , 1971; Heinrich, 1974b; Rat'kova,
1975). Significant seasonal changes also occur in the California
Current (Walsh et al . , 1974).

The greatest changes in trophic relationships should occur when a
period of relative stability is replaced by a period of upwelling of water,
and vice-versa. Apparently, at the beginning of upwelling of the water
one can expect a delay in grazing and underutil ization of phytoplankton,
particularly since these regions are dominated by relatively large, slowly
developing Copepoda. Probably, in these communities the underutil ization

123

of phytoplankton is less strongly expressed than in the neighboring neritic
communities, but more strongly than in oceanic communities. In the band
of great abundance of large herbivorous Copepoda, located along the edge
of the shelf in the region of the Peru Current, there is quite intensive
grazing of phytoplankton even when in the neighboring neritic region the
concentrations of phytoplankton are high, and it is clearly underutilized
(Heinrich, 1974b).

124

6. Deep-Water Communities.
(M. E. Vinogradov)

Communities of the meso-, bathy- and abyssopelagic zones live below
the producing surface zone of the ocean and inhabit basically the inter-
mediate, deep and benthic waters.

Energy dependence. Communities inhabiting waters below the euphotic
zone have practically no producers of their own. In a few regions,
chemosynthesizinq bacteria act as producers, but the organic matter
which they form plays a clearly subordinate and local role in the overall
balance of organic matter in the ocean. Thus, all communities of the
meso-, bathy- and abyssopelagic zones are energetically dependent on
communities in the producing zone and cannot be looked upon as viable
biocenoses in the meaning of Yu. Odum (see I.l).

However, there is a permanent, and at times very intensive exchange
of population between the communities of the various vertical zones. For
example, the population of interzonal herbivores in the cold-water regions
of the ocean feeding in the surface zone, descends to depths of
1000-2000 m. They make up almost half of the mass of the population of
the meso- and bathypelagic zones, and are the most important components
of both the surface and the deep-water communities. From this standpoint,
the surface and dependent deep-water communities can be considered as
a part of a single, larger community, encompassing all or almost all of
the depths of the oceanic waters, and this mass with its population can
be looked upon as a single ecosystem. Nevertheless, the population of the
mass of water is stratified, which allows us to speak of communities
characteristic for various depths, and to study their specific features.

Energy enters the communities of the ocean depths with organic
matter formed in the surface layers, in the euphotic zone. By whatever
path this matter reaches the depths of the ocean, in the form of products
of metabolism of the animals living in the higher levels or in the form of
their dead remains, in the bodies of animals performing vertical migrations,
carried down from the coast and shelf by benthic currents, in any case
the quantity of this organic matter decreases as it descends into the
deeper layers due to consumption by the population of the intermediate
depths and mineralization. Therefore, as depths increase, the population
of the pelagic zone finds itself living in conditions of ever-increasing
food shortage. The concentration of plankton decreases with depth
roughly exponentially.

In those regions of the ocean where the productivity of the plankton
of the euphotic zone is higher, the quantity of deep-water plankton is
also higher, and the change in the structure of its communities with depth
is slower than in oligotrophic regions.

125

The quantity of deep-water plankton may be influenced not only
by the production in the euphotic zone, but also by the balance of life
cycles of the surface communities, which determines the degree of utili-
zation of this production within the communities of the euphotic zone
itself (Banse, 1964). The lack of experimental determinations of the
ecologic and physiologic characteristics of deep-water plankton prevents
us as yet from testing this statement. If the structure of the deep-water
communities differs beneath water areas with differing balanced cycles
of surface plankton, this dependence may not arise at all (Vinogradov,
1958).

At the ^ery least, in the temperate and cold water regions of
the ocean the flux of organic matter from the surface layers into the
depths undergoes seasonal cyclic variations. The seasonal unevenness
of delivery of food, obviously, must cause seasonal variation in the life
cycles of deep water fauna. Actually, even at ultra-abyssal depths
(below 6000 m) in the waters of the Kuril -Kamchatka trench, seasonal
variations in the age population structure of certain pelagic animals
have been detected (Vinogradov, 1970a).

We should not forget that as depths increase, not only the quantity
of food, but also its nature, changes. As a result, the type of nutrition
of the main mass of plankton changes, and there is a change in the
dominant trophic groups with depth. All of this significantly influences
the species and spatial structure of deep-water communities.

Tendency to decrease energy expenditures. In the highly productive
boreal regions of the Pacific Ocean, phytoplankton fixes approximately 110 c
of carbon for each square meter of surface each year, while in the oligo-
trophic central waters of the tropical zone, carbon fixation is only
28 g, i.e., some 4400 and 1100 g of wet organic matter is produced
beneath each square meter each year (Koblents-Mishke, 1965). If we know
the distribution of biomass of zooplankton in the world ocean and assume
that its production in the subpolar waters is 1.5 times greater (Yashnov,
1939), and in the tropical waters is 7 times greater (Steemann Nielsen,
Jensen, 1957) than the maximum biomass, we can calculate that for the upper
200 meter layer in both regions the ratio of primary production to pro-
duction of zooplankton (Pp/Pz) is approximately 45-50, i.e., 1 gram of
production of zooplankton requires 45-50 g of production as wet organic
matter in the phytoplankton. Riley (1951) believes that only 10%
of the organic matter produced in the surface zone ever gets below the
200 m level. Considering this information and assuming that the annual
production of the deep-water plankton is approximately equal to the biomass
or somewhat less, it is easy to see that at depths of 200-1000 m, the ratio
of Pp/Pz in the subpolar regions is 3-5*, in the tropics--ignoring

*The biomass of plankton in the 200-1000 m layer includes the upper
interzonal species. Excluding these, the Pp/Pz ratio will be approximately
doubled.

126

macroplanl<ton--20, considering macroplankton, approximately 8-10. In other
words, animals living at lower than 200-1000 m receive approximately 5-10
times less energy per unit of biomass than animals in the surface layers.
If we compare the energy balance of the surface animals and the animals
living below 1000 m, the difference will be still greater.

It should be kept in mind that interzonal migrating species feeding
in the surface layers represent a significant fraction of the plankton
only down to depths of 500-1000 m. At greater depths, particularly in
the tropical regions, their significance decreases rapidly and the
unique food relationships of the oligotrophic bathypelagic zone are
clearly seen.

In the food-rich surface layers, even significant energy losses,
related to the active movement of the animals, can be comparatively easily
compensated for by increasing the intensity of feeding. In the poorer
deep waters, this is not always possible. It is believed (J0rgensen,
1966) that the energy expenditures of plankton filter feeders are expedient
only if the quantity of organic detritus which can be assimilated from the
water is over 25 mg/liter. Actually, the quantity of organic detritus
in the deep waters is 0-32 mg/liter as protein equivalent, or 0-70 mg/liter
as organic matter.

Adaptation to existence under conditions of extremely scarce food
resources in groups having different types of nutrition may be manifested
differently and to a different extent. However, the tendency to reduce
the expenditure of energy is inherent in the entire population of the
depths. The upper and interzonal animals, which spend only a part of
their life cycle in the deep waters, decrease their metabolic level
sharply at this time. For example, Calanus hyperboreus, which descends
in the winter to a depth of 500-2000 m, decreases its energy expenditure
for respiration by a factor of 3. This change in the intensity of
respiration is purely adaptive and is independent of temperature. Calanus,
remaining in the deeper layers for the winter, is in a unique state of
anabiosis (Conover, 1962).

As the depth increases and the food resources decrease, the mean
dimensions of animals change. They increase significantly for predators and
certain other forms in the bathypelagic zone. In the abyssopelagic zone,
the role of predators, as we have stated, is gradually reduced to nothing
and, therefore, the mean size of zooplankters decreases (Vinogradov, 1968).
The increase in the dimensions of carnivorous forms results not only from
predominance of representatives of larger genera of animals, but also from
deep-water gigantism. The essence of this phenomenon is an increase in
the dimensions of animals of the same genus or similar genera with increasing
depth. For example, in various species of the genus Serges tes, the mean
dimensions increase from 27 mm (S. vigilax--habitat 110-6b0 m) to 94 mm
(§-• lobustus^-- habitat 550-800 mmT; for Taaningichthys , the corresponding
figures are from 65 mm (T. minimus--mean depth of habitation 475 m)
to 95 mm (T. paurolychnus--mean depth 900 m); for euphausiids of the genus
Stylocheiron--from 6 mm (S. suhmi--mean depth 25 m) to 30 mm (S^. maximum--
mean depth 550 m). Attempts have been made to explain this phenomenon by
the effects of various abiotic factors, primarily pressure and temperature

127

(Wolff, 1956; Birshtein, 1963; Belyaev, 1966). However, V. B. Tseytlin
(1975) has shown that the primary factor determining the increase in
dimensions of zoophagous forms with depth is the decrease in the quantity
of food resources available. The drop in temperature also plays some
role. Based on food consumption and its variation with temperature,
V. B. Tseytlin has developed a method for estimating changes in the
dimensions of similar species of carnivorous animals with increasing
depth and decreasing food concentration and temperature. The results
produced correspond well to those observed in nature.

In nonpredatory groups, changes in dimensions are more difficult to
follow, but it has been noted that in the abyssopelagic zone, smaller
forms predominate than in the higher layers. This is probably related to
the fact that the fine filter feeders, which satisfy their demands with
smaller quantities of foods, have an advantage there. The decrease in
the mean dimensions of filter feeders does not result from a decrease in
the size of species in the genus--their dimensions may even increase, as
in the case of the predators--but rather due to predominance of genera
with smaller species.

The principle of economy of energy expenditures leads to radical
restructuring of the entire organism (Denton, Marshall, 1958; N. B. Marshall
1960; Walters, 1951; Vinogradov, 1968; etc.). The basic adaptations move
in the direction of creation of neutral buoyancy, so that the animal can
remain in the suspended state without expending muscular effort, thereby
decreasing the rate of active metabolism.

The comparatively good food supply for fishes found in the surface
zone allows them to lead an active mode of life. Preservation of buoyancy,
which is near neutral, with extreme changes in depth of habitation (and,
consequently, hydrostatic pressure) and temperature of the environment is
possible only by active, rapid changes in the volume of the swim bladder.
This requires well developed musculature, a strong skeleton for the
attachment of this musculature and a system for rapid liberation of oxygen
from the blood into the swim bladder and for its rapid absorption by the
blood. All of this requires significant energy expenditures. Active
hunting is possible only with high mobility, while developed sense
organs (particularly vision), a complex brain structure, strong musculature,
and, consequently, intensive metabolism. All of this draws a basic distinc-
tion between the nekton inhabiting the rich epipelagic and mesopelagic
layers from the true deep-water residents.

In fish which do not rise into the surface zone and live at depths
of over 500-1000 m, as well as most of the deep-water pelagic invertebrates,
neutral buoyancy is achieved by means not requiring additional expenditures
of energy. A decrease in specific weight is achieved primarily by
reduction of the content of heavy tissues. The bony skeleton is replaced
by a cartilaginous skeleton, and muscle fibers are weakened. The sub-
cutaneous layers and spaces between muscle fiber bundles are filled with
gelatinous mesenchyma, and a portion of the subcutaneous cavities--with
fat. Most of the soft tissues are gelatinous in consistency, as a result

1?8

of which the mean content of water in the tissues of deep-water fishes
is 2.5 times higher than that of shallow-water species (Walters, 1961).
The swim bladder loses its main purpose, that of maintaining neutral
buoyancy with changing pressure, and either disappears completely or is
reduced and filled with fat. The tissues of the bladderless bathypelagic
fishes are 2-4 times poorer in protein than those of the shallow-water
species (Denton, Marshall, 1958). The decrease in basic metabolism also
results from a reduction in the sensory organs.

The reduction in musculature leads to simplification of the circula-
tory and excretory systems. In deep-water pelagic fishes, the surface of
the gill leaflets is greatly reduced, decreasing the respiration rate.
The low rate of respiration and secondarily simplified excretory system
indicate a low level of metabolism and a corresponding decrease in energy
expenditure. And, in fact, measurements of the metabolic rate of certain
deep-water fishes at the depth where they live have shown that it is two
orders of magnitude lower than that of shallow-water fishes of the same
size (Smith, Hessler, 1974).

The weak development of musculature and the systems of organs which
serve it and the low rate of metabolism are possible only with extremely
limited mobility of the animals. Deep-water animals are almost all
predaceous, but cannot be predators which actively seek out and chase their
prey, but rather only passively attracting predators. This has been
confirmed by direct observations. For example, J.-M, Peres, observing the
behavior of Chauliodus sloanei from the bathyscaphe, writes, "These fish
float motionless in the water, the longitudinal axis of the body inclined
at an acute angle to the horizontal, so that the head is higher than the
tail. The long second ray of the dorsal fin, equipped with a luminous
organ, is extended forward above the head, so that the tip of the ray is
in front of the mouth." Cyclothone and Gonostoma are "always immobile,
floating passively; they wait for their prey, rather than following it; I
saw no motion of the fins, with which they maintain their equilibrium"
(cited by Marshall, 1960, p. 110, 107).

In many deep-water Decapoda, the carapax are much thinner than in
the animals living higher up; let us compare, for example, Hymenodora
frontal is, with its comparatively hard external skeletons, and the deeper-
water species H_. glacial is , the external skeleton of which is quite fragile,
or the strong Systellaspis and Oplophorus with the \/ery fragile Notostomus,
etc. In the deep-water cephalopod mollusks (Vampyroteuthis, Vitreledonel la,
Amphitretus , Japetella, Eledonel la , etc.) have lost most of their supporting
and muscular tissue. A thick layer of jelly-like subcuticular tissue has
developed, while the muscles have partially degenerated and are also
replaced by jelly-like tissue, so that the consistency of these cephalopods
is similar to that of medusae. Thus, even the large inhabitants of the
depths are passive planktonic animals, not active nektonic animals.

Passive waiting, rather than active hunting, for food is characteristic
of deep-water invertebrates as for deep-water fishes. This is indicated,
in particular, by the (sometimes greatly) elongated extremities, allowing

129

testing and feeding in a large volume of water by cephalopods and crus-
taceans, and the weak development of the eyes of deep-water decapods and
mysids. For example, Chiroteuthis and Mastigoteuthis have greatly
elongated tentacles, which may be 5 or 10 times as long as the body. The
anterior appendages of certain predaceous deep-water Copepoda are greatly
enlarged by lengthening of the segments of the basipodite of the second
maxiliipeds and have sparse but long, strong setae. In a living specimen
(Wickstead, 1962), the feeding appendages are extended downward and
forward and form a trap which snaps shut whenever prey enters it. However,
the predaceous copepods do not attempt to follow prey which floats past.

Thus, the adaptations related to the peculiarities of existence
and attempts to reduce the expenditure of energy are quite radical and
varied. They change the appearance of pelagic deep-water animals much
more than do adaptations to changes in other factors of the environment.
In other words, changes in the food supply, not changes in physical
parameters such as light, pressure or temperature, are most important in
determining the peculiarities of morphology of the pelagic animals at
different depths.

The principle of economy of energy expenditure is apparently not
limited to a decrease in the level of basic and active metabolism. In
the opinion of V. Walters (1961), one important path of evolution in
waters poor in food resources, such as at great depths, is neoteny.
Neotenic development eliminates the catabolic phases of the life cycle
and the morphogenesis of "mature" structures. As a result, the animals
need less energy for the attainment of sexual maturity.

Peculiarities of the breeding of deep-water animals are also related
to the acquisition of food. Two paths of development of juveniles are
possible for inhabitants of the food-poor deep waters: either production
of a large number of small eggs, with the small, weak larvae feeding in
the food-rich surface zone, or the production of a small number of large
eqgs, rich in vitellus, so that the embryos can pass through a number of
metamorphic stages before hatching. The large, lecithotrophic larvae,
when they first hatch, need not (or almost need not) feed, if there is
no suitable food available, and later are capable of utilizing large,
scattered food objects, which could not be eaten by planktotrophic larvae.
The former path is characteristic for most deep-water pelagic fish. The
latter has been followed by only a few, primarily benthic, deep-water
species (certain Apoda, some of the Macruridae, Liparidae, etc.), although
this path is followed by the overwhelming majority of deep-water higher
crustaceans (Decapoda, Amphipoda, Euphausiacea, Mysidacea, etc.) and
many Cephalopoda.

The direction of evolution is also related to a great extent to the
food resources: Where food is abundant, highly fertile species are
primarily produced, with short life cycles and a broad range of adaptation,
while under conditions of limited food supply, relatively less fertile,
narrowly specialized species with long life cycles are found (Shmal 'gauzen,
1968). The abundance of food resources also defines the structure of the
pelagic communities at various depths.

130

Considering the above facts and data on the variations in quantity,
specific composition and predominance of various trophic groups (II.l)
with depth, we can attempt to provide a brief description of the structure
of the communities of the meso-, bathy- and abyssopelagic zones.

Mesopelagic zone (20O-750:-100O m). Most of the population consists
of species directly related to the surface zone and feeding in it during
their ontogenetic or diurnal migrations. The concentration of zooplankton
here, in some cases, particularly in temperate and cold-water regions, is
almost as great as the concentration in the surface layers. In addition
to the migrating animals, bacteriophages are also important (Radiol aria,
Phaeodaria, etc.), utilizing the high concentration of bacteria and single-
celled heterotrophs, usually found at depths of 500-700 m (Sorokin,
1971a). In addition to migrants (carnivores and herbivores), predatory
forms which do not migrate to the surface layers are also significant
(see II.l). The communities are highly varied, almost equal in species
to communities of the surface zone in the tropics and more varied than
communities in the cold-water regions.

Bathypelagic zone (750^1000-3000 m). Communities are characterized by
comparatively low population and biomass, no greater than 20-30 mg/m3, even
in the most productive regions of the ocean, with significant predominance
of carnivores over detritophages and herbivores, among which, in the cold-
water regions, the upper-interzonal filter feeders are still important.
In the upper levels of the bathypelagic zone, they may make up as much as
30-40/^ of the mesoplanktonic biomass.

The main mass of the population consists of predatory forms,
utilizing the organic material which enters this zone from the surface
zone. However, most of the predators are passive--they do not chase
their prey, but rather attract it. The sparsity of the food resources and
the need to reduce the expenditures for active and basic metabolism lead,
in many groups, to significant morphologic restructuring. As a result, the
fauna differs taxonomically from the surface fauna. This is particularly
true of groups present in the surface layers as active predators, in the
bathypelagic zone as species which have gone over to passive waiting for
food (Birshtein, Vinogradov, 1971).

The variety of the community is great; many groups of pelagic animals
reach high species diversity here. The lower population, with comparatively
larger number of species, means that the dispersion of the distribution of
individual species is significantly greater than at lesser depths.
The increase in the diversity index of communities indicates an increase
in stability, which, according to Margalef (1963b), allows the community
to continue its existence with a smaller quantity of energy entering the
system, i.e., with more limited food resources.

Abyssopelagic zone. Communities inhabiting depths over 3000 m have
been \jery little studied. The biomass and number of plankton are
extremely low, and decrease with depth. No group has its maximum species
abundance below 3000 m. In contrast to the bathypelagic community, the

131

abyssopelagic community might be called oligomictic. The extreme
sparsity of plankton, apparently, makes even passive predation energetically
inexpedient, and carnivorous species almost disappear. The plankton at
these depths consist primarily of small detritophages or omnivores. The
species poverty of the abyssopelagic zone results also from the fact that,
given the great sparsity of the population, the dispersion of the dis-
tribution of individual species increases so greatly that the sexes do
not encounter each other sufficiently frequently to breed. The population
of the greatest depths, having the lowest total number, can exist only
with comparatively homogeneous species composition.

132

CHAPTER III. BENTHIC COMMUNITIES AND THEIR
STRUCTURAL AND FUNCTIONAL CHARACTERISTICS

1. Littoral Communities. (0. G. Kussakin)

The boundary of the ocean is generally considered to be the line of
zero depth, representing the lowest possible tide for a given area
resulting from purely astronomic causes. However, the influence of the
ocean is wery strongly felt along the shore at points located slightly
higher than the zero depth line. Therefore, the intertidal zone and
supralittoral areas, although they are located above the zero level, i.e.,
formally belong to the land, are considered zones of the sea.

The intertidal zone, or drying zone, is defined as the zone located
between the high and low tide marks. Thus, its lower boundary is the
zero depth level, and its upper boundary is the highest theoretically
possible tidal level. Consequently, the intertidal zone is a zone which is
periodically flooded with water, and periodically exposed, subjected to
the action of the air. The amphibiotic nature is its most characteristic
feature. Although its vertical extent is extremely small (from a few
centimeters to 16 m in the Bay of Fundy), if the shoreline has a gentle
slope the width of the intertidal zone may be as much as several kilometers.
No matter what the width of the intertidal zone, the degree to which it
is amphibiotic changes a great deal from its top to its bottom; therefore,
the conditions for the life of littoral organisms change a great deal over
a small distance. In spite of the fact that the intertidal zone is a
zone which is transitional between the land and the sea, the overwhelming
majority of its population consists of marine plants and animals, although
in certain places, particularly those protected from the surf, specialized
forms of land organisms predominate--marsh halophytes and mangroves.

Its boundary position between the two main habitats of life--the
air and the water--and the amphibiotic conditions present there distinguish
the intertidal zone among all other zones of the sea. The daily and
seasonal fluctuations in temperature, salinity, moisture content, etc.,
are most sharply reflected here. Great expanses of the coastline in
the Antarctic, Arctic and temperate latitudes are covered in winter
with ice which, on the one hand, has a destructive, abrasive influence,
but on the other hand, protects the inhabitants of the intertidal zone
from the effects of the extremely low air temperatures.

Above the intertidal zone is the supralittoral zone, which is also
subject to the influence of the ocean, though to a lesser extent. This
zone is flooded with water only sporadically, during strong onshore winds
or severe storms. The rest of the time, the supralittoral is irregularly

133

wetted by spray from the surf, and in friable soils, by capillary rise
of sea water. In this area, the forms of terrestrial origin predominate
as to number of species (insects, arachnids, flowering plants, etc.),
although in the quantitative aspect, specialized forms of marine origin
may dominate (Talitridae Amphipoda, in the tropics--crabs, etc.).

1 .1 Zonal ity of the Intertidal Zone

The Question of the principles of vertical subdivision of the
intertidal zone into systems of coordinated units of lower rank has been
discussed approximately since the middle of the last century. The expe-
diency of this type of subdivision is beyond doubt, since the vertical
stratification of organisms and their complexes is particularly clearly
manifested in the intertidal zone, and frequently, particularly if the
shoreline is not broken, groups of flora and fauna (communities) may
extend almost without interruption for hundreds of kilometers, forming
clear stripes but a few decimeters or even centimeters in width. However,
the question of the principles upon which the subdivision of the inter-
tidal zone should be based remains in dispute.

It would seem most simple to accept the biotic principle, i.e., to
divide the intertidal zone in accordance with the communities or types
of communities--formations forming the strips along the shoreline, which
we observe in nature, particularly since they are not distinguished by
great variety. The overwhelming majority of schemes of this type,
however, have reflected the specifics of only a limited sector of the
shoreline and are therefore only of historic interest. The greatest of
the schemes of this type is the universal scheme of zonal ity suggested
by T. A. and E. Stephenson (Stephenson, Stephenson, 1949) for a rocky
intertidal zone. The Stephensons subdivide the intertidal zone into
three "zones," each with its own typical inhabitants, usually relating
to the same life forms, but with different species or genera in the
different regions: the supral ittoral edge, or the littorine zone; the
middle littoral zone or the barnacle zone; the sublittoral, or infra-
littoral edge. Later, an attempt was made (Dahl, 1953) to provide a
similar system for an intertidal zone with friable sediment. One signifi-
cant shortcoming of such a system, like others based only on the distribu-
tion of organisms, is the failure to give proper weight to the significance
of tidal variations in sea level as the primary factor defining the
vertical distribution of the organisms and their communities in the
intertidal zone. Furthermore, harder sediments, sand and mud do not
have common communities; therefore, the systems developed for different
sediments are different and difficult to compare and, finally, the
leading groups of any sediment, if they are cosmopolitan, may be located
at Quite different levels, due to differences in temperature and salinity
of the water, insolation, surf power, etc. Furthermore, even under
similar conditions, the vertical distribution of indicator species is
not always constant. For example, in the British Isles, the upper
boundary of the middle intertidal zone, defined according to the upper
boundary of massive accumulation of barnacles, is significantly higher
where Chthamalus stellatus predominates than where Balanus balanoides,
which lives at a lower level, dominates. Thus, systems based on indicator
organisms and their communities cannot yield universal vertical boundaries
for subdivision of the intertidal zone.

134

Of the abiotic factors acting on the composition and distribution
of littoral communities, the most important, essentially determining the
specifics of the intertidal zone as an independent zone, are the tidal
fluctuations in sea level. The relationships between the durations of
periods of immersion and exposure to air in different parts of the
intertidal zone determines, basically, the vertical stratification of
organisms and their communities in this zone, which is manifested quite
clearly in all climatic zones. The principle of relating the vertical
boundaries within the intertidal zone to the levels of the neap and
spring tides, as well as the mean sea level for European shores with
true semidiurnal tides, was first clearly formulated by L. Vaillant
(1891), then later successfully used by a number of researchers (Pruvot,
1897; Beauchamp, 19U; Gurjanova et al . , 1925. 1930a, b). According to
this principle, the intertidal zone is subdivided into three horizons,
of which horizon II, or the middle horizon, is bounded by the mean low
water stages and mean high water stages, while horizon I, the upper
horizon, and horizon III, the lower horizons are determined by the
boundaries of the littoral itself. Each horizon is divided into two
stages, the boundaries of the stages being the mean high water and the
mean low water springs for the upper and lower horizons, while the
middle horizon is divided by mean sea horizon. The use of the principle
of Vaillant, developed for an intertidal zone with true semidiurnal
tides, is quite difficult in those coastal areas where other types of
tides occur. P. V. Ushakov (1951) has shown that the principle of
Vaillant is applicable to conditions of irregular semidiurnal tides, but
the boundaries of the stages are defined differently: In horizons I and
III, these boundaries are the mean high water and mean low water springs.
We consider that the principle of Vaillant can also be applied to inter-
tidal zones with diurnal and irregular diurnal tides, although in these
cases it is not the levels of the springs and neaps which are characteristic,
but rather the levels of the tropical and equinoctial tides (Kussakhin,
1958a, 1951). It is interesting in any case to subdivide the middle
horizon into two stages with a boundary at mean sea level.

With this expansion of the principle of Vaillant in all cases the
upper horizone of the intertidal zone remains above water most of the
time, exposed to the air for several days in a row (during the equinoctial
or neap tides). Conversely, the lower horizon spends most of its time
beneath the water, and is exposed only during the lowest (spring or
tropical tides; the middle horizon, with all types of tides, is character-
ized by periodic daily immersion and drying out. Similar conditions will
be observed in corresponding stages with all types of tides.

In addition to the tidal fluctuations in sea level, the vertical
stratification is greatly influenced by the force and constancy of the
surf. An increase in strength of the surf usually results in shifting of
the littoral communities upward. Sometimes, this displacement may be as
great as several meters vertically; in these cases, the entire intertidal
zone may be occupied by purely sublittoral communities, with the true
littoral community shifted far upward. Of the biotic factors, competitive
relationships may greatly influence the vertical distribution of organisms.
In many cases, there may also be seasonal changes in stratification of
communities, with this type of displacement observed in all climatic zones.

135

Schemes like the scheme of the Stephensons, which combine the
characteristic features of vertical stratification of the basic communi-
ties, can be used only in comparative ecologic studies, always in com-
bination with subdivision of the intertidal zone according to the principles
of Vaillant.

Of course, when used in this manner, the terminology of the Stephensons
must be slightly altered, since the "zones" of the Stephensons--the
supral ittoral edge, the middle littoral zone and the sublittoral edge--are
not considered by us to be the primary subdivisions of the intertidal zone,
but only characteristic types of formations of rocky facies of the
intertidal zone. We consider it expedient to call them systems or divisions.
Since the term "middle littoral zone" might be easily confused with the
middle, or second, horizon in the system of Vaillant, we propose to apply
the term "true intertidal zone" or "true littoral division" (eul ittoral)
to this division.

In nontidal seas, like the Black Sea and Baltic Sea, where there is
no true (tidal) intertidal zone, there are communities quite similar to
littoral communities, though their vertical stratification is much less
fully developed. In these seas, there is a special zone, which has come
to be called the pseudol ittoral , which owes its existence to the surf waves
(Mokiyevskiy, 1949). 0. B. Mokiyevskiy accepts the upper edge of the
maximum surf spread as its upper boundary, the lower edge of the beach,
where the surf wave is obstructed, as its lower boundary.

1 .2 Factors Specific for the Littoral

The nature of the connection between the sea coast and the ocean or
open sea has a great influence both on the abiotic conditions of the littoral
environment, and on its population. Open, unprotected shores are usually
subject to strong surf action, the surf becoming weaker with increasing
distance from the ocean, and practically disappearing in partially closed
bays and lagoons. The role of the surf in the conditions of the intertidal
zone is very significant and quite varied. First of all the surf, wetting
the intertidal zone partially neutralizes the effect of the tidal factor,
particularly at low tide. This decrease in amphibiotic conditions in the
intertidal zone under the influence of the surf means that as the force and
constancy of the surf increase, the vertical stratification of littoral
communities becomes decreasingly tied to the tidal levels, since in surf
areas they extend higher up the shore than in protected areas. In areas
with strong surf, this upward shift may reach 2-6 m (Burrows et al . , 1954;
Kussakin, 1961 •, Vozzhinskaya , 1955). Also, as a wave breaks and the
layers of water are mixed, the water is enriched with oxygen, frequently
to the point of supersaturation. This encourages the existence of many
oxyphilic animals in areas where there is surf.

However, the surf also has a harmful mechanical effect, washing away
organisms which are not tightly attached. In loose sediments, the surf
helps to wash organic matter out of the sediment and causes motion of
sediment particles. Therefore, on beaches with surf, even though the
oxygen mode is favorable, the food value of the sediment is frequently low.

136

Depending on the amount of surf action to which a shoreline is
exposed, various authors distinguish from 4-5 (Beauchamp, 1914; Lewis, 1964)
to 8 (Ballantine, 1961) types of shores. The scheme of degrees of surf
action recognized by Soviet investigators of the intertidal zone is as
follows (Gurjanova et al . , 1930a, b; Kussakin, 1958a, 1961; Gurjanova,
1968).

First degree--closed bays, no surf;

Second degree--partially closed bays, well protected shore, surf
very rare and wery weak;

Third degree--less protected shore, surf frequent, but weak due to
comparatively great distance from open sea;

Fourth degree--open sea, surf almost constant, but not great due to
comparatively mild acceleration of waves;

Fifth degree--open sea shore, almost constant strong surf, great
acceleration of waves;

Sixth degree--open ocean shore, continuous, strong surf, \/ery great
acceleration of waves.

It must be emphasized that the degree of surf action depends not only
on the distance of the shore from the open sea, but also on the topography
of the shore and morphology of the substrate. If a shoreline is greatly
broken, even on an open sea coast, there are always areas which are
protected to some extent from the surf. This is observed most clearly
in areas of scattered rocky reefs and banks of pebbles and boulders.
Even the different sides of a single lump of rock differ in the degree
of exposure to the surf and may be populated by different communities.

The composition of littoral communities depends to a great extent
on the nature of the sediment. The population of loose sediments depends
largely on sediment particle size, mobility, degree of grading, water
content in the sediment and the quantity of organic matter present. In
surf habitats on loose sediments, there are no macrophytes or almost none,
and relatively little microscopic algae. Therefore, the basic food for
the inhabitants of sandy beaches, in addition to plankton, consists of
allochthonic organic matter (detritus and algae thrown up on the beach).
In habitats protected from the surf, where the loose sediment has been
silted, there are usually rather rich stands of eelgrass and, in the
tropical zone, mangrove as well. In sandy sediments, infauna predominates
over epifauna, but in surf habitats it is also quite sparse. Gravel and
rocky beaches are still more sparsely populatied.

The population of rocky and stony sediments is significantly more
varied. Here, green, brown and red algal macrophytes are usually well
developed, with a rich fauna of small mobile animals, plus settlements
of sestonophages (barnacles, oysters, mussels). The great biomass of
the macrophytes is mostly not eaten by the phytophagous animals; most of

137

it dies and is transformed to detritus. Thus, stony and rocky intertidal
zones are distinguished by significantly greater primary production
than consumption, whereas the opposite is true of intertidal zones with
loose sediments.

On all sediments, particularly rocky sediments, sestonophagous
animals (barnacles, bivalves, ascidians, sponges, coelenterata , many
higher crustaceans, etc.) are quite important. In the Murman intertidal
zone mussels and balani make up 55-90% of the total animal biomass (Kussakin,
1963). Therefore, the role of the pelagic zone as a food resource for
the population of the intertidal zone is exceptionally important.

The composition of littoral communities is also influenced by the
petrographic composition and morphology of the substrate. It has been
shown that changes in the abundance of algae and barnacles are freauently
related to variations in the hardness of the rock (Moore, Kitching, 1939).
Hard granites and gneisses, even where the surf is strong, can support
large Laminaria and Fucuses which attach to them (Gurjanova et al.,
1930a, b). Phoronis larvae select primarily sandstone to settle on.
When loose soils are close to rocks, this results in silting and
accumulation of sand, which also influences the composition of littoral
communities. Slightly jointed rock masses, particularly cliffs exposed
to the surf, maintain rather homogeneous and relatively sparse populations.
The number of bands here is usually minimal, and there are few animals
except for barnacles and bivalve mollusks. Conversely, the more broken
up the rock, the richer the population it can support. The presence of
pools, clefts, niches, overhangs and grottoes creates a variety of
conditions of illumination, wetting and protection from the surf. In
these areas, the littoral communities are particularly rich and varied.
Here we also see a general upward movement of communities into higher
levels and movement of certain sublittoral inhabitants into the intertidal
zone.

The influence of ice on the littoral biota is both harmful and
favorable. The negative influence of ice is primarily a result of its
mechanical wearing effect. It is manifested most strongly in an inter-
tidal zone with surf, particularly where the morphology of the coast is
simple and the ice is in constant motion. In these areas, the population
is entirely destroyed in the winter, then after the ice melts, ephemeral
(spring, summer or autumnal) or annual communities develop, with pre-
dominance of diatoms and small macrophytes (Chordaria , Pterosiphonia,
Polysiphonia , Porphyra , Cladophora, Acrosiphonia) . As the wearing effect
of the ice becomes weaker, conversely, the significance of communities
with predominance of multiannual forms such as laminaria, focuses
or Sargasso algae increases (Gislen, 1930; Stephenson, Stephenson, 1954;
Kussakin, 1958h). Where the coastline is broken, only individual projecting
sections of rock are exposed to the action of the ice. Apparently, the
significant changes in the composition of communities observed with various
degrees of surf action result not only from the variations in tolerance
of plants and animals of the surf itself, but also their resistance to
the wearing effects of ice.

138

On the other hand, an ice cover, particularly where it remains
almost immobile throughout the winter, isolates the inhabitants of the
intertidal zone from the effects of the \/ery low air temperatures during
low tides, and the harmful effects of winter storms. This positive
influence of ice cover allows many warm-water species to tolerate severe
winter conditions and is, along with the great warming in the summer,
one of the main reasons for concentration of thermophilic faunal and
floral elements in areas protected from the surf.

Climatic conditions also have a great influence on the intertidal
zone. A mild oceanic climate with slight seasonal and diurnal variations
in air temperature, cool, wet summers with abundant fog and moderate
winters are most favorable for the inhabitants of the intertidal zone. In
regions with this type of climate--the Komandorskie Islands, Kerguelen
or Macquarie--the intertidal zone is richly populated (Gurjanova, 1935;
Ushakov, 1958), since many sublittoral species rise into the intertidal
zone. Conversely, in areas with hot, dry summers or cold, long winters,
the littoral communities are usually sparse, particularly multiannual
algae, which cannot leave the intertidal zone during the unfavorable
seasons. Therefore, in the tropics, the algoflora has a tendency to
shift downward to the lower horizons of the intertidal zone or into the
sublittoral (Gurjanova, 1961a; Mokiyevskiy, 1964, 1967).

The time of day at which low tide occurs is of great significance,
particularly in countries with hot, dry seasons (Stephenson, Stephenson,
1972). For example, in the intertidal zone of Ghana in the summer the low
tides occur at night, and as a result, regular penetration of certain
mass species of algae into higher horizons is observed. In the winter,
the lowest tides are observed in the day, resulting in a lowering of the
upper boundary of a number of algae (Lawson, 1957, 1956). If fog is
frequent during low tide, this has a favorable influence on the littoral
biotope. The orientation of the coast is also important, as it determines
exposure to sunlight, as is the steepness of the shore. Southern exposures
and gentle slopes are more strongly subject to the drying influence of
the sun than are northern or steep (i.e., shaded) shores. In countries
with monsoon climates, strong rains may cause the death of many littoral
organisms if they occur at low tide.

1 .3 Typology of Intertidal Zones

In our opinion, the most convenient and acceptable classification of
intertidal zones is that based on bionomic types developed by E. F.
Gurjanova, I. G. Zachs and P. V. Ushakov (1930a, b). Following the prin-
ciples which they developed, we can distinguish six bionomic types of
intertidal zones.

First bionomic type (moderately protected shore). Characterized by
second or third degree surf. Good aeration, salinity usually high,
but may be lower near rivers. Distinguished by the greatest richness
and variety of littoral communities, the vertical stratification of

139

which coincides most closely with the horizons and stages distinguished
on the basis of tidal levels. This type includes many bays, the interiors
of certain gulfs, as well as areas of open but broken coastlines pro-
tected from strong surf.

Second bionomic type (open sea shore). Characterized by fourth or
fifth degree surf. Salinity approximates normal oceanic; conditions of
aeration good, water frequently supersaturated with oxygen. The harmful
mechanical effect of the surf predominates over the useful effect. The
bands of plants and animals are shifted upward, and many of the bands
characteristic for areas with weaker surf are absent.

Third bionomic type (open ocean coast). Characterized by maximum
Surf, strong and constant wetting of entire intertidal zone by spray,
even during lowest tide; the harmful effect of the surf is so great that
the population is greatly impoverished, but the most enduring forms,
having no competition, extend almost throughout the intertidal zone.
There is often practically no precise vertical stratification. The
communities of the sublittoral edge are shifted upward and occupy
almost all or even all of the intertidal zone, while the littoral
communities themselves are usually located in the supral ittoral zone,
which is constantly wet by the surf and spray.

Fourth bionomic type (lagoons). Characterized by total absence
of surf (first degree surf) and extensive development of mud and sandy
sediments. Salinity usually depressed to some extent, but elevated in
countries with arid climate.

Fifth bionomic type (estuaries). Surf usually absent, less frequently
second or third degree. Salinity greatly reduced, and usually changes
with the phases of the tide. An estuarine intertidal zone is an area in
which the continental, marine and fresh-water biota come together.

Sixth bionomic type (pools). We include here all depressions and
large indentations in rock, as well as the pools left between rocks and
on beaches at low water. This type is characterized by absence of surf
or a reduction in the harmful influence of the surf, while retaining its
aerating influence, remains quite wet even during the lowest tides,
and has a complex hydrologic mode. The temperature and salinity of the
water frequently change greatly. One specific feature of pools is that
water is constantly present, even if they are located in the supral ittoral .
This means that the conditions of existence in pools are similar to those
of the sublittoral, except that the variations in hydrologic factors are
significantly greater than in the sublittoral zone. The main factors
determining the composition of the population of pools are their position
above the zero depth level, the nature of the sediment, the size and
particularly the depth, the effects of wind and surf, the peculiarities
of their connection with the sea during low tide (if there is any such
connection), the degree of influence of continental runoff, steepness
of the walls, nature of change of hydrologic factors and illumination.

140

Of the many attempts which have been made to classify pools, the
classification of T. Gislen (1930) seems most suitable to us. This
classification divides them into sublittoral, intertidal zone, and
supralittoral types. Sublittoral pools are usually located in the lov;er
horizon of intertidal zones and are usually washed by waves and surf or
are connected with the sea by narrow channels. Their population is
basically similar to the sublittoral population. Littoral pools are
connected with the sea during high tide or when wave action is strong.
The changes in temperature and salinity in these pools are significantly
greater than in the sea. Their population is usually quite varied; in
addition to typical sublittoral and littoral species, forms are also
seen which are found only in pools. Supralittoral pools are connected with
the sea only during maximum high tide, and sea water enters these pools
only in the form of surf spray and storm waves. After strong rains, the
water is sometimes almost entirely fresh, while during hot weather, con-
versely, the salinity may be higher than that of the sea. The temperature
fluctuations are also quite great. The fauna and flora of these pools
includes a few eurybiotic marine representatives, plus a specific popu-
lation made up of brackish-water and even fresh-water, frequently ephemeral,
species.

Pools are found in all of the other bionomic types of intertidal
zones; therefore, many authors do not distinguish them as a specific
bionomic type, but rather consider them specific habitats (Newell, 1972)
or as separate biotopes (Zhyubikas, 1969) within each of the remaining
bionomic types.

1 .4 General Characteristics of the Littoral Biota of the
World Ocean

We noted earlier that in all climatic zones and on all sediments,
clear vertical stratification of organisms is a characteristic of the
intertidal zone. On relatively unbroken, morphologically homogeneous
shores, the communities are located in bands, strips frequently extending
over great distances, but always relatively narrow. They can be easily
distinguished on a rocky shore, and are less clearly seen, but still well
expressed, on shores consisting of loose sediment. This type of distribution
is called linear, or banded.

Some believe (Gislen, 1943; Gurjanova, 1947, 1959, 1961a) that the
banded distribution of groups (communities) is primarily characteristic
for the intertidal zone in the temperate and higher latitudes, with a
mosaic distribution predominating in the lower latitudes. This is explained
by the more acute interspecies competition in the tropical intertidal
zone, a result of the increased number of species attempting to populate
a single level or sublevel (Gurjanova, 1961a). Nevertheless, even in the
tropics, the banded (linear) distribution of littoral communities is quite
common. On the other hand, even in the temperate zones, where the
morphology of the shore is complex, a number of "inserted," supplementary
communities appear, and the banded distribution is replaced by a spotty
or mosaic distribution.

141

Along a stony, or particularly rock-cliff intertidal zone, in
areas where the shoreline is quite broken, the population is varied. A
single rock or column may manifest differences in the quantity, composition
and vertical position of the band-forming communities on different sides,
with different exposures to the waves. On cliffs extending out into
the open sea, the communities are quite different from those on cliffs
protected from the surf, and in sections of rock projections located
near sandy beaches, the composition of the population is altered in
comparison to clean rocks. In areas where fresh water runs down the
rocks, the quantity of brown and red algae decreases sharply, the green
or blue-green forms becoming dominant. In clefts in the rock, in
grottoes or beneath overhangs, communities similar to sublittoral
communities develop in abundance, or sponges, Actinea, Ascidia, etc.,
may be encountered in abundance in these areas alone. On flat reefs
with many breaks, large numbers of pools, puddles and depressions are
left at low tide. The banded distribution is completely disrupted in
these areas, since the pools and depressions have their own communities
(sometimes several communities in each pooll), depending on the position
of the pool, its depth, the nature of the bottom, etc. Since one or
two, less frequently three, species predominate clearly over the others
in rocky littoral communities, the appearance of each community can be
easily distinguished from the others. Therefore, the variety of the
communities is easily seen. In one rocky high boreal intertidal zone
in open Kronotskiy Bay, not distinguished either by variety of bionomic
types or by richness of species of fauna and flora, in 1970 we found no
less than 27 band-forming groups, clearly different as to dominant
species.

Thus, for an intertidal zone great changes in communities in the
vertical direction and great variability of communities under the influence
of local factors are both characteristic. Considering the great local
variability, we assume that the littoral biota is almost infinitely
variable. Nevertheless, the intertidal zone in almost all regions of
the earth, under bionomically similar conditions, supports communities
which dre of the same type or quite similar, with a limited selection of
the very same, either variant or morphologically similar species. As a
result, the great variety of littoral communities, upon careful examination,
is found to consist of a small number of regularly repeating series
of similar communities. Following the lead of botanists (Feldmann,
1951) and certain hydrobiologists (e.g., Dellow, 1950), these series
should be called formations.

R. Bolin (1949) believes that the linear distribution of littoral
organisms, where almost each individual is peripheral, greatly increases
the chances for survival of mutants and gives the organisms high evolu-
tionary potential. This, in his opinion, is one important reason for
the tremendous richness of species in the intertidal zone. However, if
we exclude the large number of 1 i ttoraloxene species, which dre atypical
for the intertidal zone, the number of littoral species is relatively
low. On the average, the number of species of animals in an intertidal
zone is 1/2-1/4 the number in the upper sublittoral, although the environ-
ment there is generally less variable. Apparently, this results from the
fact that only the most eurybiotic species can exist in the intertidal
zone and supra! ittoral zones. These species, which have great ecologic

142

plasticity and d.re polymorphous, i.e., capable of forming various
intraspeci fie (hereditary and nonhereditary) biologic groups, have great
evolutionary stability. From the standpoint of the theory of ecologic
stability, the eurybiotic species are evol utionarily more stable than
the stenobiotic species (Jackson, 1974; Eldredge, 1974).

The following peculiarities of the intertidal zone can be added to
those already discussed. It is characteristic for the intertidal zone
that the types of communities (formations) are limited, finding homologs
and analogs on all coasts of ttie world ocean. Possible exceptions
include the cryocenoses of the Arctic and Antarctic and the mangrove
areas of the tropical zone (Golikov, 1975a). These littoral communities
consist of a relatively small number of eurybiotic, polymorphous,
ecologically plastic but evol utionarily stable species.

These peculiarities of the intertidal zone have been reflected in
the figurative words of L. A. Zenkevitch: "The intertidal zones of the
various coastlines of the earth represent a play, with the same parts,
which are played in different places by different actors."

As to degree of similarity (and in many cases of kinship), littoral
communities can be divided into four groups.

1. Identical communities. Groups of organisms occupying similar
biotopes within a single biogeographic province or area, less frequently
a single climatic zone, the dominant species of which Are the same. We
must not forget that in terms of its specific composition, one and the
same community is far from identical, not only in its remote regions,
but also frequently in neighboring regions. In extreme cases, the
composition of a single community in different biotopes of a single
region may have almost no common species except for the dominant species
itself, plus a few banal species common to the entire intertidal zone.
For example, on the northwest coast of Iturup Island, a community of
Cystoseira crassipes algae is found, however, of 17 species of
macrophytes which make up the community, only two are common to the
cliffs and the rocks, including the band- forming species, and of 45
macrofaunal species, only four are found on both the cliffs and the
rocks (Kussakin et al., 1974).

2. Parallel or vicariant communities. Groups of organisms
occupying similar biotopes within different zones, biogeographic areas
or provinces, with closely related dominant species, usually of one
genus, less frequently of one family or superfamily (Thorson, 1957).
These vicariant communities frequently dominate throughout an entire
biogeographic dtveA. As an example, for the boreal zone we can cite the
communities of Chthamalus stellatus, Pelvetia canal iculata , Fucus

di stichus , Li ttori na obtusata , Testudinal ia testudinal is, Gammarus
oceanicus + Li ttorina saxatil il s , Halosaccion ramentaceum , Rhodymenia
palmata ,~Alaria esculenta + Laminaria digitata on the rocky European
coasts and the corresponding communities of Chthamalus dalli, Pelvetia
wrighti i , Fucus evanescens, Littorina kurila, Collisella cassis,
Anisogammarus locustoides + Littorina sitchana , Halosacc ion glandiforme,
Rhodymenia stenogona, Alaria angusta + Laminaria bongardiana in the
intertidal zone of the fareastern coast of the USSR.

143

Comparison of the specific composition and biomass of the
macrobenthos of the communities of brown algae Fucus distichus.
characteristic for the middle littoral of the boreal zone in the North
Pacific--the lower boreal (southern Kurile) and higher boreal (eastern
Kamchatka) zones--shows that, in spite of the fact that eastern
Kamchatka and the southern Kurile belong to different biogeographic
subareas, the specific composition of the communities of _F. evanescens
is quite similar--54 species are common, something less than 2/3 of the
number of species in each of the regions compared, their biomass making
of the total biomass of the macrobenthos in the community
A quite different picture is observed as we compare the
of the vicariant communities of _F. distichus and £. evanescens

biomass (84-86.5% of total biomass) is

up 94-98%
(Table 1)
structure
(Table 2)
accounted
than half

Here, most of the
for by the vicariant species, although they represent less
of the total number of species present in the community. The
common species present is not great, the degree of similarity,

number of . .

as defined by Jnccard, is only 11.8%, increasing somewhat (to 14.6%) if

we compare the communities of the higher boreal regions alone.

Table 1. Changes in the composition of the community Fucus evanescens in various
biogeographic provinces.

Eastern Kamchatka, higher Southern Kurile, lower
boreal littoral. Total boreal littoral. Total
biomass 4534 g/m^ biomass 4879 g/m^

Categories of
Species

No. of % of total Biomass No. of % of total Biomass
Species No. of % of Species No. of % of
Species total Species total

Species common

for both regions

54

Vicariant

species

16

Species found

only in one re-

gion vicariance

17

Undefined species
Total species

62

18

20

98(35)'

1
0.1

54

18

16

61
21

18

87

94

(9)*

1
5
5

♦Parentheses show biomass excluding dominant species F. evanescens.

3. Convergent or isomorphic communities. Groups of organisms occupying
similar biotopes, the dominant species of which are not closely related forms,
but belong to the same life forms. For example, in the upper intertidal zone
of the tropics, Littorinidae hv^i. frequently replaced by Neritidae, while

the middle intertidal zone, the prosobranchial mollusks (of the families

in

144

Tdble 2. Comparison of the structure of parallel communities of Fucus
distichus and Fucus evanescens.

Fucus distichus community: Fucus evanescens community

ithe

2

coast of Mirman. Total eastern Kamchatka and southern
Categories biomass 9133 g/m^ Kurile

of species Average total biomass 4707 g/m

No. of % of total Biomass No. of % of total Biomass
species No. of % of species No. of » of
species total species total

Species common
to both com-
munities 19 31 5 19 16 8

Vicariant

species 30 48 84(12)* 42 36 85.5(12)*

Species with

no vicariance 13 21 11 57 48 5.5

Undefined

species - - 0.1 - - -

Total species 62 - - 118

*Parentheses show biomass excluding the dominant species _F. distichus or F.
evanescens.

Patellidae and Tecturidae) are replaced by the externally quite similar
pulmonata Siphonari idae.

4. Functionally analogous communities. The dominant species in
these communities are not related, and belong to different life forms,
but are in the same trophic group. For example, the communities of
filter feeders such as barnacles or mussels, common for the intertidal
zone, may be replaced by communities with predominance of other filter
feeders--sponges, simple Ascidia of the family Pyuridae, colonial
Ascidia of the family Polycl inidae , tubular polychaetes of the family
Sabellidae, etc.

1.5 Supral ittoral Biota

The population of the supral ittoral is extremely homogeneous. For
solid sediments, the crustose green and blue-green algae ( Calothrix ,
Plectonema , Enthophysal is) and crustose lichens (Verrucaria, Lichina,
Lithoicea, etc.) are typical . The fauna here are mixed in origin.
Typical land forms include insects (tochilidae, Staphyl i nidae, Diptera),
pseudoscorpions, red mites, as well as myriopods. The algal wastes

145

contain many ol igochaetes. Of the forms of marine origin, most
characteristic dre specialized families of amphipods, isopods, decapods,
and gastropods. Typical are isopods: Porcellio scaber, species of the
genera Halophiloscia , Detonella, Trichoniscus and particularly the most
primitive of the isopods, found only on the sea coast, the Ligiidae
(genus Ligia). Of the amphipods, for loose soils the Talitridae (genera
Tal itrus, Orchestia, Talorchestia , Orchestoidea) are characteristic. On
various soils, gastropods diVe encountered, primarily the Truncatel 1 idae
and Assimineidae (Truncatella , Cecina , Assiminea , Ovassiminea , etc.).
For the tropical supral i ttoral on friable soils, the running crabs
Ocypode, Sesarma, etc., land hermit crabs Coenobita and representatives
of a special suborder of isopods, the Tyloidea (Tylos, Hel leria) are
quite characteristic. The Tylos species inhabit the coastlines of our
seas as well--the Black Sea and Japan Sea.

Clusters of blooming vegetation develop in silty soil, such as the
glassworts (Sal icornia, Plantago maritima, Arthrochemum, etc.) and, in
the tropics, mangroves.

A significant portion of the animals in this zone are scavengers.
According to 0. B. f'takiyevsky (1969), the biomass and population of
species of land origin in the supral i ttoral are both low, not over a few
tenths of a gram per m'^. Groups of marine origin, particularly the
Talitridae, provide much of the biomass in the temperate zone: up to 1
kg/m , with a population density of as much as a hundred thousand
individuals per m^. In the tropics, the biomass of the Ocypodidae and
Coenobita is rarely over a few tens of grams per m^ (^tokiyevsky, 1969).

1.6 Littoral Biota. Rocky Intertidal Zone

The communities of the supral i ttoral edge in areas with weak or
moderate surf usually occupy the upper stages of the highest horizon of
the intertidal zone and the lower portion of the supral ittoral zone.
Most characteristic for this area Are the Littorinidae gastropods, and,
in the tropics, the Neritidae. Therefore, the supral ittoral edge is
frequently called the littorine zone. The supral ittoral wood lace Ligia
is also frequently found here.

In the lower boreal European intertidal zone (La Nbnche, coast of
Britain), below the supral ittoral zone there is usually a band of
lichens of almost black color, dominated by Verrucaria maura and Lichina
conf inis. In the lower portion of the lichen band, the quantity of
Littorina neritoides and _L. saxatil is increases, as well as mites, the
springtails Petrobius maritimus and the shore isopods Ligia oceanica.
Of the algae, in areas of surf, films of blue-green algae develop
(Calothrix, etc.), plus small green algae and the red algae (Ulothrix ,
Urospora, Bangia), in places the larger Porphyra and Enteromorpha . In
the lower portion of the supral ittoral edge, we always begin to see
species characteristic of the upper portion of the eul ittoral section:
Pelvetia canal iculata , Fucus spiralis, Lichina pygmaea, less frequently
Chthamalus stellatus and Fucus distichus (Lewis, Powell, 1960; Lewis,
1972) . TrT protected habitats, the width of the supral ittoral edge is
only a few centimeters, but on an open coast, it is greatly expanded by
the action of the surf.

146

On the high boreal intertidal zone of Europe, we do not find
Littorina neritoides or Ligiidae. On the rocky intertidal zone of
I'lurnian, _L. saxatil is dominates, the amphipod Hyale prevosti and oli-
gochaetes are seen. In surf habitat, usually the green algae (primarily
Urospora penicill ifonnis) , blue-green alagae and a few Porphyra
umbil ica'l is are found (K^ssakin, 1953). The biomass of algae here is
usually not over 200 g/m^, of animals--! g/m^. On the rocky intertidal
zone of Kurman, the biomass of algae (Ulothrix pseudoflacca and
Spongomorpha sp.) decreases to 30 g/m^, the biomass of animals increases
greatly--to 150-650 g/m^--due to the increase in the number of _L.
saxatil is (up to 1600 indiv./m ) and the appearance of a large number of
amphipods, primarily Gammarus oceanicus (>10,000 indiv./m ).

In the northern Pacific in the boreal zone, very similar
communities are developed with predominance of J., si tchana, J^. kurila
and L. mandschurica , gradually replacing each other in that sequence
from north to south. On littoral cliffs of the Kurile, the density of
Littorina kurila reaches 15,000 indiv./m^, with a biomass of up to 2
kg/m^, while in rocky littoral areas we find up to 100,000 indiv./m^,
with a biomass of up to 15.5 kg/m^.

In the subtropical and tropical latitudes, in addition to the genus
Littorina, we also find other representatives of the family
Li ttorinidae--Melarapha , Nodil ittorina , Granul ittorina , Tectarius ,
Echinella, Peasiella, Echininus and Bembicium. Sometimes, several

species of Littorinidae form independent bands at the supral ittoral
edge. For example, in Tanabe Bay (Japan), bands of Nodil ittorina pyra-
midal is , H_. granularis , _N. picta , Littorina brevicula and, finally,
Peasiella roepstorff iana follow in sequence from top to bottom (Habe,
1958) . Tn addition to the Littorinidae, the Neritidae and Grapsidae
crabs are also characteristic.

The littoral system per se. This system, in places with moderate
or weak surf, is usually located between the mean levels of high water
and low water springs or tropical tides and occupies a large portion of
the intertidal zone. The population of this system is significantly
more varied than that of the supral ittoral edge, but here also we
encounter only a few formations over a considerable area, flost charac-
teristic are the barnacles (Chthamalus , Balanus, Tetrad ita , Elminius ,
Lithotrya, Ibla , Octomeris, etc.), limpets Tecturidae, Patelidae and
Si phonoari idae, the predaceous gastropods Thaididae, the mussels
Mytilidae ( Mytilus, Brachyodontes, ffediolus, Septifer, etc.) and the
Ostreidae (Ostrea, Crassostrea, etcT) and the Grapsidae. Usually here
we also find Littorinidae and Neritidae, particularly in the upper
portion of the system, but here they are rarely among the dominant
species. In places, the polychaete Serpulidae or Sabellidae, sea
urchins (Paracentrotus , Strongylocentrotus , etc.), ascidian Pyura, etc.,
may predominate. Among the algae, the green, brown, and red are well
represented. In temperate waters, the brown algae usually predominate--
the fucoids (in the North Atlantic Fucus, Pelvetia, Ascophyllum, in the
northern portion of the Pacific Ocean Fucus, Pelvetia, Pelvetiopsis , in
the southern hemisphere Hormosira). In warm seas, the red algae usually
dominate, and in temperate waters they are numerous in the lower
intertidal zone.

147

The domination of various animals and plants within the intertidal
zone itself and their vertical distribution Are closely related to their
competitiveness and endurance for external factors. The small barnacles
Chthamalidae settle higher than the larger Balanidae, and of the latter,
such large species as Balanus cariosus settle lower than the smaller _B.
balanoides, less capable of competing with the mussel and fucoids.

The geographic vicariate is also rather clearly expressed, although
in different oceans the vicariant species have essentially different
areas of distribution. For example, Chthaiiialus stellatus extends in the
north to Great Britain, whereas its Pacific vicariance Ch. dalli extends
no further than Olyutorskiy Bay. In contrast, Pelvetia canal iculata
reaches the shores of Murman, while its western Pacific Ocean vicariance
_P. wrighti i extends only to Iturup Island. Many littoral organisms are
also asymmetrically distributed with respect to the poles. Thus, Patel-
lidae and Si phonari idae in the northern hemisphere do not extend farther
than the lower boreal waters, whereas in the southern hemisphere they
dre characteristic not only for the Subantarctic, but for the low
Antarctic as well .

The lower boreal coast of Europe characteristically features
communities of Chthamalus stellatus + Bostrychia scorpioides and the
lichen Lichina pygmaea, extending into the uppermost portion of the
intertidal zone. The J., pygmaea community is among the few littoral
communities in which most of the animals feed on the dominant plant. To
the north, _Ch^. stellatus is gradually replaced by Balanoides balanoides,
which settles somewhat lower. Characteristic inhabitants of barnacle
communities in the lower boreal intertidal zone of Europe Are the
Patel la spp. limpets. In some places, particularly those protected from
the surf, the Fucoidae dominate, usually forming several bands--Pel vetia
canal icul ata in the upper intertidal zone, then Fucus spiral is , still
lower _F. distichus or _F. vesiculosus. With further weakening of the
surf, the Fucusae are frequently replaced by great clusters of
Ascophyllum nodosum. In the lower portion of the littoral system, a
varied community of small algae usually develops, primarily the red
algae (Laurencia pinnatifida, Gigartina stellata. Coral 1 ina officinal is ,
Lomentaria articulata, Membranoptera alata, Pulmaria elegans,
Rhodymenia palmata), as well as brown al gae Xi-eathesia difformis, some-
times _F. serratus) . With an increase in surf power, the fucoid cover
becomes less prevalent, and the quantity of Mytilus edulis increases; in
the lower intertidal zone, the brown algae Himanthalia elongata and
Bifurcaria bifurcata frequently dominate. In habitats with heavy surf,
the lower portion of the littoral is dominated by 1 i thothamnion, Balanus
perforatus and Patella aspera (Southward, 1958).

The composition of the true littoral communities in high boreal
waters of the coast of Murman and the White Sea in its general features
is the same, but the species composition is impoverished. The number of
bands of fucoids is reduced due to the disappearance of the communities
of Fucus spiralis, _F. edentatus and Pelvetia canal iculata. The
Patellidae are replaced by Testudinalia tesselata. In the intertidal
zone of flirman, below the supral i ttoral edge, a community of
Porphyra umbilical is + Balanus balanoides usually develops, with some
green al gae Enteromorpha intestinal is . etc . , Li ttorina saxatil is . Hyale

148

prevosti and Oligochaetae (Kussakin, 1953). The lower band of
Fucus vesiculosus is clearly seen only in areas with moderate surf.
There dre usually few animal s--_B. balanoides and L. obtusata predomi-
nate, f'tost characteristic for the true intertidaT zone of Murman is the
community of Fucus distichus. For the lower portion of the eulittoral
system, communities of small algae, primarily red algae, are
characteristic. They sometimes form a mosaic continuum. The fauna here
is much more varied than in the fucoid communities: Between the
thallomes of small algae, we find small mollusks, isopods, amphipods,
polychaetes, etc. In the habitats below _F. distichus, protected from
the surf, Ascophyllum nodosum develops.

Predominance of the same _B. balanoides , Mytilus edulis and fucoids,
with the number of bands of the latter in the intertidal zone still less
than in Murman, and with some reduction in the number of species, is
characteristic for the White Sea. Below the communities of
Porphyra umbil ical is + Q_. balanoides, there is usually a well developed
band of Fucus vesiculosus, still lower--a band of Ascophyllum nodosum.
Of the animals, the mussels usually predominate clearly, while Ej_
balanoides, L. obtusata and L. littorea Are also rather numerous.

In the boreal zone of the Pacific Ocean, we find quite similar
communities, though more varied in specific composition, although for
certain formations (e.g., the fucoids) we find exceptions. The main
"characters" here are also the mussels (_fl. edul is , _M. cal ifornianus) ,
the barnacles (Chthamalus dalli, _B. cariosus, _B. glandula, _B. balanoides
and _B. crenatus) and the fucoids. The selection of fucoids is not as
rich here as in the North Atlantic: Fucuis evanescens (similar to the
Atlantic _F. distichus) , Pelvetia wrighti i , _P. fastigiata and
Pelvetiopsis limitata.

For the surf intertidal zone of the Bering Sea coast of Chukotka,
multiannual algae are typically absent due to the long, severe ice
cover. A significant portion of the intertidal zone itself is occupied
by the community Porphyra pseudol inearis + Urospora penicilliformis +
Bacillariophyta, while in places communities of Scytosiphon dotyi +
Petalonia fascia + Pylaiiella littoralis develop. In the lower portion,
we sometimes observe a belt of Halosaccion compressum with H.
glandiforme and Iridaea cornucopiae intermixed. Of the animals, oli-
gochaetes predominate, less frequently amphipods. The biomass of
animals is never over 20 g/m^.

The intertidal zone of Anadyrskiy Bay is quite poor, both qualita-
tively and quantitatively, but further to the south, in the direction of
Olyutorsky Bay, the arid zone is gradually enriched and takes on
features characteristic for a high boreal intertidal zone in the far
eastern seas. The intertidal zone of eastern Kamchatka is populated
quite richly and can be characterized as a typical high boreal
intertidal zone of the northwestern Pacific (Spasskiy, 1961). The high
boreal type of intertidal zone is also well represented by a large
portion of the coast of the Sea of Okhotsk, south to Cape Terpenia and
Friz Bay, and also along the Pacific coast of the Kurile to the south to
Yekaterina Bay. The intertidal zone of the individual sections of the
continental coast of the Sea of Okhotsk has been described by P. V.

149

Ushdkov (1951) and 0. B. f-bkiyevskiy (1953), of the Shdntarsky Islands--
I. G. Zdchs (1929). For the upper portion of the intertidal zone itself
in the northern Sea of Okhotsk, bands of Gloiopeltis furcata and
Heterochordarid abietina + Myelophycus intestinale with a sparse fauna
consisting primarily of Littorina sitchana and Chthamalus dalli, and
particuldrly, settlements of bdrndcles-- Ch. ddll i . Q_, crendtus dnd _B.
bdldnoides--dre most chdracteristic.

Extensive development of banks of Mytilus edulis are a
characteristic feature of the littoral of the continental coast of the
Sea of Okhotsk, giving it features of external similarity to the White
Sea intertidal zone. The number of mussels is usually great among
stands of fucus, but the clusters of mussels descend to horizon III,
where they are frequently quite dense. In addition to the mussels,
settlements of fucus are often seen in the lower portion of the
eulittoral system, while the formation of varied, usually mosaically
arranged small algae, primarily red and brown algae, is most common.
The biomass of plants in the communities of the upper portion of the
eulittoral is 150-800 g/m^ in stands of Gloiopeltis capillaris, 250-800
g/m in the band of Heterochordarid abietina + Myelophycus intestinale.
up to 3-4 kg/m^ in the group of Porphyra ochotensis and up to 5 kg/m^ in
the band of Halosaccion gldndiforme (Vozzhinskdyd, 1965, 1957; Blinova,
Vozzhinskaya, 1974). An equally high plant biomass is seen in associa-
tions of fucus, Corall ina pil u1 iferd dnd various red algae--up to 4-9.5
kg/mS

In the northern and centrdl Kurile, in the upper portion of the
littordl system, communities of Gloiopeltis furcdtd,
Porphyra umbil ical is , Acrosi phonia , 81 indingia , ftinostroma , and in
places Heterochordarid abietina usually develop. Barnacles do not
settle here. Mast characteristic for the middle portion of the system
are stands of Fucus evdnescens, or if the surf is strong--
Balanus cariosus settlements with biomass of up to 21 kq/n/ (Kussdkin et
dl., 1974) . STTght development of Mytilus edulis is chdrdcteristic.
For the lower portion of the littordl system, the red algae Rhodymenia
stenogona , Rhodomela larix, Rhodoglossum japonicum, Iridaea cornucopiae,
Ptilotd asplenioides are characteristic, while the characteristic
animals are the gastropods Littorina kurila. Lacuna reflexa,
Nucel la freycineti , Buccinum percrassum, _B. baeri , Col 1 isella spp.,
primarily _C. cdssis, the bivdlves Vildsind vernicosd, Turtonid minuta,
the polychaetes Nereis vexillosa, Chone teres, the crdbs
Pdgurus hirsutiusculus and P. inTddendorf f i , the isopods Idotea aleutica
and a large number of dmphipods. In the middle Kurile, hermit crdbs dnd
isopods are absent.

In the southern Kurile, southern Sakhdlin and the northern portion
of the Japan Sea, right down to Nevel'skiy Bay, the intertidal zone is
of lower boreal type. The overall appearance of the communities of the
eulittoral is retained, but it is characteristic that the upper portion
of the system contdins bdnds of Chthdmdlus ddlli and the fukoid
Pel vetia wrightii , while the lower portion features certain warm-water
dlgde. There is d grddudl disappeardnce of the high boredl species,
repldced by vicarious low boredl species. Furthermore, general
enrichment of the specific composition of the fauna is observed. The

150

peculiarities of the low boreal intertidal zone are most clearly
expressed along the coast of southern Primor'ye, where the tidal range
is short, and where Fucus evanescens disappears, and Pelvetia wrightii
becomes more rare, h'ost characteristic for the upper portion of the
littoral are Littorina mandshurica and j.. brevicula , a band of
Gloiopeltis furcata, sometimes forming mixed stands with _H. abietina ,
and a band of Chthamalus dal 1 i , while in the lower section we see mosa-
ically distributed stands with predominance of red algae.

The high boreal intertidal zone of the Pacific coast of America has
a great deal in common with the high boreal intertidal zone of Asia.
However, due to the less severe winter conditions here, there is a
significant influx of warm-water species, e.g., the crabs Pugettia,
Oregonia and Cancer. The high boreal intertidal zone, characteristic,
in particular, for the Aleutian Islands and the Gulf of Alaska, begins
to be replaced by a low-boreal intertidal zone (much more gradually than
along the coast of Asia) around Vancouver Island and the northern
portion of the coast of the state of Washington. The typical low boreal
intertidal zone of northern California extends with slight variations to
Cape Conception (Ricketts, Calvin, 1961; Stephenson, Stephenson, 1972).

In southern California, the intertidal zone is of subtropical type,
although with some boreal aspects, a result of the relatively cold water
which washes this coast even in summer. The southern features are
introduced with settlements of the gastropods Vermetidae--
Spiroglyphus lituellus and Altes squamigerus, the relative abundance of
the trochids Norrisia, Tegula funebralis, T. ligulata, the turbinids
straea undosa and the bivalve mollusk Pseudochama exogyra. Calcareous
red algae are also abundant in the lower portion of the intertidal zone.

Along the coast of Asia, the lower boreal intertidal zone extends
to the south approximately to Cape Inubo and Sado Island along the coast
of Japan and to Wan San along the coast of Korea.

Along the northwestern coast of Honshu Island, the intertidal zone
is a transient type between low boreal and subtropical, the boreal
Chthamalus dalli being replaced by the subtropical

Chthamalus challengeri (Hoshiai et al., 1965). The intertidal zone of
Sagami Bay on the Pacific coast of Honshu is of subtropical type,
although there is some intermixture of boreal species and genera, e.g.,
Strongylocentrotus (Gislen, 1943). Of the barnacles, Balanus amphitrite
and Tetrad ita squamosa are characteristic for the uper portion of the
intertidal zone, of the al gae--Monostroma , Sargassum thunbergi and
Turbinaria, for the lower portion-- Chondrus + Gigartina, stilT lower--
Corallina + Pachyarthron + Laurencia with the characteristic craboid
Petrol isThes Japonicus. A community of _Ch^. dal 1 i is still retained on
the rocky intertidal zone of the Yellow Sea, but is mixed with many
subtropical species. Lower down are belts of oysters and ulva algae
(Gurjanova et al . , 1958). In the eastern China Sea, we observe massive
development of warm-water cirripedian crustaceans Tetrad ita squamosa
and Mitella mitella (Mokiyevskiy , 1967). In the southern China Sea on
shores with surf and high salinity, coral reefs develop, though they are
sparse. The remains of ancient colonies of coral which have died are
still more commonly seen.

151

Further south, along the cliffs of the Indo-China peninsula, in the
upper portion of the intertidal zone there are few algae, but a rich
population of settled animals (actinea, serpulids, the barnacles
Tetrad i ta porosa , Balanus and Chthamal us, complex ascidians, the
oysters Ostrea forskal i and _0. spinosa) , and in the lower portion the
algae Turbinaria, Padina, sargassums and calcareous red algae such as
Melobesia develop (Fischer, 1952).

In Indonesia, the Nerita rise quite high in the intertidal zone.
The distribution of fauna is quite variegated and mosaic. The
overwhelming portion of the intertidal zone carries low biomass--a few
grams, less frequently a few tens of grams per m^ (Mokiyevskiy , 1967).

Along the coast of northern and northeastern Australia, there dre
extensive coral reefs extending into the intertidal zone. In the upper
portion of the intertidal zone itself are settlements of Chthamal us ma-
layensis and Ch. withersii with occasional isopods. Below this are
bands of Crassostrea amasa. Tetrad ita squamosa and a narrow band of
Acanthozostera and Liolophura or Acanthopleura. Still lower we see the
simple ascidians (Microcosmus austral is), Chthamalus caudatus.
Tetrad ita costata, sponges, Siliquaria ponderosa, crabs, holothurians
and the algae Valonia and Padina (Stephenson, Stephenson, 1972). In
southern Australia and Tasmania, settlements of Chamaesipho columna.
Chthamalus antennatus and Catophragmus polymerus develop, plus bands of
Modiolus pulex and Brachyodonte rostratus. In the lower portion of the
intertidal zone there is usually a band of Galeolaria caespitosa
(Bennet, Pope. 1953).

Along the intertidal zone of the Subantarctic island of Macquariae,
there are apparently no barnacles; the most characteristic vegetation is
Porphyra umbil ical is with some Ulva lactuca. Enteromorpha intestinal is
and other algae. The lower portion is dominated by Rhodymenia. Of the
animals, the gastropods Siphonaria lateralis, Nacella delesseri and
Macquariella hamiltoni are most common (Stephenson, Stephenson, 1972).

The sublittoral or infral i ttoral edge. This level usually occupies
the lower portion of the zone which dries out, and when the surf is weak
corresponds to the lower stage of horizon III of the intertidal zone.
Independent communities are formed rather rarely here; more frequently,
communities of the upper sublittoral simply extend into the zone.
However, due to the drying of the edge, though it may be brief, its
population differs from the sublittoral population; first of all, the
specific composition is much more sparse. Secondly, certain strictly
littoral species are present. In cold and temperate waters, large
laminaria algae predominate, while in warm waters we usually see the
upper boundary of the colonies of corals, dense clusters of the ascidian
Pyura, and stands of Sargassums and red algae are encountered; at all
latitudes, calcareous Rhodophyta are seen here, belonging to various
genera, but usually called 1 i thothamnion (cortical and branched, nonseg-
mented forms) and corallina (branched segmented forms). Frequently, in
warm waters, these calcareous red algae develop quite rapidly and form
massive "bridges" or "trotoires" (in the Mediterranean) or even entire
reefs (in the tropics). The porous or spongy thallomes of these plants
provide shelter for numerous cryptofauna. In warm waters, calcareous

152

m

Chlorophytd are also common, for example, Hal imeda , but their signifi-
cance in the formation of reefs is much less. In rocky places, communi-
ties of sea grasses (e.g., Phyl 1 ospadix in the northern Pacific) are
found, although they Are more characteristic for looser beds. On the
whole, the sublittoral edge is the most varied portion of the intertidal
zone in terms of specific composition. It is here that we find signifi-
cant numbers of species from the groups of animals which dre not charac-
teristic for the intertidal zone, as are the Echi nodermata , Ascidia,
sponges, Bryozoa, Cephalopoda, Brachyopoda, fish, etc.

In the boreal intertidal zone of the Atlantic Ocean, the
development primarily of laminaria algae, to a lesser extent red algae
and fucuses, is characteristic. Of the animals, the most common Are
Mytil us edul is , the gastropods Testudinalia tessellata,
Li ttorina 1 i ttorea , Nucella lapillus, the sea urchens Strongyl o-
centrotus droebachiensis , the sea stars Asterias , the sea anemone
Teal ia. Where the surf is weak, the laminaria are frequently replaced
by Fucus serratus stands.

The high boreal eastern Atlantic sublittoral edge is quite poor in
species composition. For example, the Patellidae are practically absent
here. Nevertheless, the main band-forming species remain the same:
Alaria esqualenta , Lami naria di gi tata , l^. saccharina, Nytil us edul is ,
Fucus serratus and the Rhodophyta.

In the northern Pacific, fucus is absent in the sublittoral edge,
but the zone of laminaria is usually well developed. In surf intertidal
zones of the Bering-Sea coast of Chukotka, typical communities of the
sublittoral edge are not found; only associations common with the inter-
tidal zone of seasonal and ephemeral algae develop here. In the inter-
tidal zone which is protected from the surf in Krest Bay, a community of
Laminaria bongardiana appears, and extends to the south along Kamchatka,
the northern and middle Kurile. Along the coast of eastern Kamchatka,
in places there is a well expressed band of laria angusta, while on the
northern and central Kurile there is also a community of
Laminaria longipes and Cymathaere triplicata.

On the littoral coast of the Sea of Okhotsk, the composition of
macrophytes of the sublittoral edge is quite different--
Laminaria longipes and Alaria praelonga are characteristic only for
southwestern Kamchatka, while further to the north and west,
Lessonia laminarioides, Laminaria gurjanovae and _L. saccharina are most
typical. It is interesting that Cystoseira crassipes is also present,
although most of its stands are located in the sublittoral
(Vozzhinskaya, 1965; Blinova, Vozzhinskaya , 1974). In the lower boreal
intertidal zone of the southern Kurile, in addition to the
1 ami nariaceans Kjellmaniel la gyrata, Costaria costata and
Arthrothamnus bifidus, stands of _C. crassi pes are quite widespread and,
to a lesser extent, Sargassum kjellmanianum and _S. thunbergi , while on
the coast of southern Skhalin we find _C. crassipes, Sargassum pallidum,
Laminaria cichorioides , J., japonica and Alaria marginata. Stands of
Phyllospadix iwatensis are also characteri<;tic for both of these
regions. Along the continental coast of the Sea of Japan,
laminariaceans extend into the intertidal zone only in places in

153

northern Priinorye, Phyllospadlx and Sargassums being characteristic only
for the upper sublittoral, while the sublittoral edge is populated
primarily by a mosaic of algae with predominance of Rhodophyta, as well
as some brown algae, particularly Coccophora langsdorffi. It is here
that the stands of 1 i thothamnions usually begin, the thickness of the
cover of which gradually increases in the sublittoral with increasing
depth. The animals here are more varied. Particularly noted is an
increase in the number of echi noderms : the stars Henricia and Leptas-
terias , Strongylocentrotus , the holothurians Cucumaria , etc. Of the
decapodes in the intertidal zone of eastern Kamchatka and the Kurile,
Thelmessus cheiragonus is characteristic, as well as juvenile
Paralithodes brevipes, etc. In the quantitative aspect, on the boreal
edge, it is not animals but plants which dominate. Only in the baths of
the Komandorskiy and, to some extent, the Kurile, does
Strongylocentrotus polyacanthus form rich accumulations, though on
reefs, frequently covered with sand, populations of the sabellids or
ascidians develop, with almost no algae.

Along the Pacific coast of North America, the sublittoral edge is
richly populated with laminaria such as Alaria val ida , _A. marginata ,
Egregia menziesi, below which we usually find Lessoniopsis littoralis,
and still lower--the sublittoral gigantic Nereocystis leutkeana,
Macrocystis pyrifera and _M. i ntegri fol ia. Also characteristic Are
Sargassum muticum, Cystoseira crassifes, _C. osmundacea and
Phyllospadix scouleri. Among the red algae, the most common are species
of the genera Iridophycus , Gigartina and Odonthal ia (Stephenson,
Stephenson, 1972).

In the temperate waters of the southern hemisphere, large brown
algae such as Durvillea antarctica, _D. wil lana, _D. potatorum, _D.
caepestipes , Lessonia corrugata , _L. nigrescens , Macrocystis pyri fera ,
species of Cystophora and Carpophyl 1 urn also develop.

A somewhat poorer laminarian flora is found in the subtropical
waters of both hemispheres, e.g., in southern California, Japan, South
America and southern Australia (species of the genera Eisenia and
Egregia) . However, most characteristic for the warmer waters Are the
calcareous red and green algae, and of the brown al gae--Sargassum ,
Turbinaria , Dictyota and Padina ; therefore, the appearance of the lower
portion of the intertidal zone is quite different from the intertidal
zone in the temperate waters. This difference is increased still
further by the departure of the coral or algal reefs or accumulation of
Vermetidae and the Polychaetae serlupids Pomatoleios and Pomantoceros ,
inhabiting the calcareous tubules of the gastropod mollusks (Southward,
1958).

1.7 Characteristic Peculiarities of the Littoral Biota of the
Tropics and Circumpolar Waters

Until recently, it was widely thought that, as we move toward the
tropics, a general tendency is observed toward descent of the littoral
fauna and flora into the deeper horizons and the sublittoral and, in
connection with that, a general impoverishment of the littoral biota
(Gislen, 1943-1944). The studies of E. F. Gurjanova (1959, 1961a,

154

1961b) and 0. B. Fbkiyevskiy (1960, 1964, 1967) have shown that this
impoverishment may be true only of algae, whereas only a few species of
animals descend in the tropics, and the indices of quantitative develop-
ment of species and biocenoses are almost equal to those of the
temperate latitudes, and in many cases even higher. The rule of domina-
tion of one or a few species is retained in the tropical biocenoses, but
at a lower quantitative level (Mokiyevskiy , 1964). As we move toward
the tropics, the specific variety of Rhodophyta and most groups of
animals increases, particularly for the crabs, sea urchins,
sipunculoids, polychaetes, gastropods and bivalves, etc. Furthermore, a
number of systematic groups of high rank, such as Pennatularia,
Scl eractinia , Alcyonaria, Zoantharia, hingeless Brachiopoda, Xiphosura,
Stomatopoda and Crinoidea inhabit the intertidal zone only in the
tropics. Conversely, some large systematic groups which inhabit only
the temperate zones Are absent (Mokiyevskiy, 1962). Only a few groups
of animals, such as the amphipods and isopods, are present more richly
in the temperate waters than in the tropics. In the opinion of 0. B.
Mokiyevskiy, the combination of conditions present in the tropical
intertidal zone results in a complex interweaving of biocenotic
connections between organisms, preventing the realization of short and,
consequently, energetically more effective food chains such as are
inherent in the biocenoses of the boreal and, particularly, high boreal
intertidal zone.

As we move toward the Arctic and Antarctic, gradual qualitative and
quantitative impoverishment of the littoral biota occurs, to the point
of complete disappearance in the high Arctic and along a large portion
of the coast of Antarctica. Since the harmful, wearing effect of
long-term ice cover is particularly strongly felt in the intertidal zone
with its surf, the impoverishment in the Subarctic is more strongly seen
in intertidal zone areas with surf than in areas with little or no
surf. This is clearly seen in the example of Anadyrskiy Bay. Whereas
on the rocky intertidal zone with heavy surf the biomass of plants
varies from 0.2 g/m^ in a community of Urospora penicilliformis to 3.8
kg/m^ in a community of Halosaccion compressum, while the biomass of
animals is only 0.5-40 g/m^ in the intertidal zone of Provideniye Bay
and Krest Bay, which are protected from the surf, the biomass of plants
varies from 88 g/m^ to 11.2 kg/m^, while the biomass of animals may
reach 13.5 kg/m^. The clear impoverishment of the littoral biota in
Subarctic-type surf habitats occurs primarily due to the complete
disappearance of perennial plants and sessile animals. That moving ice
is the culprit in this impoverishment is demonstrated by the fact that
in summer, stands of fucus or barnacles less than one year old
frequently appear here, but mature individuals remain only in clefts and
other protected habitats. Seasonal species of algae predominate in the
intertidal zone (apparently, the green filamentous algae and diatoms
extend furthest north), along with small, mobile animals, capable of
concealing themselves in the mats formed by these plants--amphi pods ,
ol igochaetes, small polychaetes, nematodes, acarines, ostracods,
harpacticoids. The mobile multiannual forms of macrobenthos also
continue to play some role (Testudinal ia , littorines, nudibranchs,
sometimes sea stars, sea urchins and hermit crabs), which winter in the
sublittoral or in concealed places. Still closer to the Bering Straits,
the population is severely depressed, even in areas protected from the

155

surf. Here, the entire littoral zone is covered with ice for several
months each year, and the few multiannudl forms which penetrate here,
such as Fucus evanescens, Mytilus edul is , Tectonatica janthostoma ,
Balanus crenatus, leave the dry zone and descend into the sublittoral.

Similar changes in the littoral biota upon transition from the
boreal to Arctic conditions have been observwed on the Atlantic coast of
North America, in Greenland (f-bdsen, 1936) and in the Barents Sea
(Gurjanova et al . , 1925). For example, in southern Greenland in the
intertidal zone itself, the zone of Balanus balanoides with bands of
Fucus vesiculosus in the upper portion and F. distichus +

Ascophyllum nodusum + Njytilus edul is in the lower portion dre still
clearly expressed. Further to the north, _A. nodosum is absent, _B.
balanoides becomes rdre and also gradually disappears, the laminarians
in the infral i ttoral edge dre replaced by mats of small algae. Along
the northeast coast of Greenland, of these multiannual forms, only _F.
distichus remains, and it also is rare (Madsen, 1935, 1940). In the
eastern Barents Sea, a gradual impoverishment of the littoral biota
occurs from west to east. Along the west coast of Novaya Zemlya, there
is still a great deal of Fucus evanescens. In the central portion of
Matochkin Shar strait, multiannual macrophytes disappear completely from
the intertidal zone and bands of Urospora penicilliformis (upper) and
Pylaiella litoralis (lower) dre seen. Along the coast of the Kara Sea
there is no macrophyta, and only at depths of 4-6 m do we see individual
Fucus distichus among the stands of laminarians.

Information on the littoral life in the Arctic itself is sparse,
and the data available dre quite contradictory. Some authors report
that the intertidal zone here is completely lifeless, while others
report rather significant numbers of species of macrobenthos for the
coastal zone. It is most probable that only cryocenoses dre present in
the Arctic intertidal zone.

The impoverishment of the littoral biota in the Subantarctic and
Antarctic occurs similarly, though with some differences. In the
southern hemisphere, representatives of the family Patellidae penetrate
clear to the Antarctic peninsula, whereas in the northern hemisphere
they are almost totally absent even in the high boreal waters.
Barnacles disappear in the Subantarctic. The intertidal zone of most of
the coast of Antarctica is apparently totally lifeless. The poor
population is observed only in the Antarctic peninsula and adjacent
islands, as well as Adelie land. In the intertidal zone of the
Antarctic peninsula, the tides are as great as 3-4 m, and in the summer
along the supral i ttoral edge, orange (Caloplaca) and black (Verrucaria)
lichens develop, in the eulittoral zone--stands of Chlorophyta Ulothrix,
Urospora , Mjnostroma , Enteromorpha , Cladophora , Chaetomorpha and the
Rhodophytd Bangia and Wrphyra (Delepine, 1966). Phytophyllic
gastropods J;fei_rga_reVU , Nacella and Patinigera polaris are found. In
places protected from the wearing effects of the ice, a rather varied
population is observed with predominance of the small bivalve mollusk
Kidderia subquadratum, which reaches a distance of 75 cm over the zero
depth level under the cover of the algae Iridaea racovitzae (Stockton,
1973). In the region of Adelie land, where the conditions of habitation
dre still more severe, the supral i ttoral edge is also populated with

156

lichens, apparently of the same species. Only two bands are clearly

seen in the intertidal zone: the upper band, formed of

Ulothrix austral is , and the lower band of diatoms, predominated by

Melosira moniliformis. Kacrophytes appear only in the sublittoral

(Delepine, Hureau, 1963). It is interesting to note that most genera of

algae in the Antarctic intertidal zone Are the same as in the Subarctic

regions.

1.8 Sandy and Silty-Sandy Intertidal Zone

In the qualitative aspect, loose soil beds ^re significantly more
sparsely populated than solid beds. The population of sandy beaches
exposed to surf is particularly sparse and homogeneous. Under Subarctic
conditions, the macrofauna is usually absent, although the meso- and
microfauna are rather widely varied. For beaches with surf in the
temperate and tropical zones, the most characteristic of the macrofauna
are the higher crustaceans: amphipods, isopods and, in the tropics,
crabs as well. Macrophytes are absent here, only microscopic algae
being present, rising to the surface of the sand for photosynthesis at
low tide and burying under the sand at high tide. As to composition of
fauna, three systems are usually distinguished on sandy beaches with
surf--the splash zone, or upper beach, which may be combined with the
supral ittoral edge of a rocky intertidal zone; the middle beach,
occupying a significant, sometimes predominant, portion of the
intertidal zone, and frequently poorest in life; the lower beach, in the
lowest portion of the intertidal zone. For the splash zone, the
amphipods Talitridae (Orchestia, Talorchestia , Orchestoidea ) are
characteristic. In the tropics, the Ocypodidae predominate,
constructing deep burrows and running after the retreating waves with
surprising speed. In warm seas, right up to the lower boreal subzone,
isopods of the suborder Tyloidea (Tylos and Helleria) Are common. The
middle beach in the high boreal waters is quite poorly populated. Kost
characteristic d.re the sand hoppers (Gammarus and Anisogainmarus ) , the
turbellarians, oligochaetes and nematodes. Primitive isopods of the
family Cirolanidae (Excirolana, Eurydice) appear in the lower boreal
intertidal zone, and Are particularly characteristic for the tropics and
subtropics. Less common here Are the polychaetes Euzonus , Ophel ia ,
Scolelepis, Nerine, Goniadides and others. The lower beach is usually
populated with a more varied and richer fauna, ("bst common here Are the
amphipods of the family Haustoriidae and Phoxocephal idae. For the
tropics, crabs of the family Hippidae (Emerita, Hippa, Arenaeus, etc.),
the bivalve mollusks Mesodesma , Amphidesma , Donax, the gastropods
Terebra , plus the crustaceans Sguilla and Callianassa are typical. For
both the wanii and temperate waters, the predaceous gastropods of the
family Naticidae, the bivalves Tivela, Tel 1 ina , Sil igua, polychaetes of
the family Nephthydidae, Glyceridae, Ariciidae and Opheliidae, mysids
and isopods of the family Cirolanidae Are characteristic. Many of these
species are found not so much in the lower intertidal zone as at the
water line, i.e., they form a migrating complex (mysids, many
Cirolanidae, Donax, some amphipods, shrimp, etc.). The biomass of
animals on sandy surf beaches is usually low, although in some places it
may be significant.

157

As the surf weakens, the population of the sandy beaches becomes
significantly richer, particularly in the lower portion. The leading
groups are usually the bivalves (Veneridae, Cardiidae, hbctridae,
Tellinidae, Myidae) and polychaetes ( Ci rratul idae, Opheliidae,
Maldanidae, Terebel 1 idae, Phyl 1 odocidae , Glyceridae, Eunicidae,
Capi tell idae). Among the gastropods, both predators and scavengers are
common, particularly Naticidae (Natica , Tectonatica , Acrybia, Pol inices,
etc.). There are also large numbers of crustaceans: in the upper
intertidal zone, the crabs and amphipods-tal itrides, in the middle and
lower intertidal zone--the sand shrimp Crangonidae, decapod crustaceans
Upogebia and Callianassa, Squill idae, the isopods Sphaeromatidae, less
frequently Cirolanidae. Macrophytes begin to appear here, particularly
in the tropics--Caul erpa , Udotea, Halimeda, etc.

In temperate waters, most of the algae do not use sand as the
substrate, but rather shells, rocks or pebbles, while some species, such
as Cladophora fracta in the White Sea, simply rest on the sand, but are
not attached to it.

Still further weakening of the surf, observed in partially closed
bays, lagoons and estuaries, is accompanied by silting of the sand and
freshening of the water. In countries with arid climates, lagoons
become brackish. For estuarine and lagoon types of intertidal zone, the
Potamogetonaceae and Hydrocharidaceae dre more common than algae. Among
the genera of the first family, Zostera is most widespread, while
Posidonia grows in the Mediterranean, and in the tropics-- Cymodocea ,
Halodule and Al thenia. Representatives of the second family, such as
Halophila , Thalassia and Enhalus , grow only in the tropical seas. The
infauna in stands of eel grass consist primarily of the same groups as
are found on sandy beaches with weak surf, but a unique fauna settles on
the leaves of the grass, containing both common phytophilic forms
(Trochidae, Turbinidae of the gastropods, Vilasina of the bivalves,
etc.) and species which are specially adapted for life on the leaves of
marine grasses, e.g., the isopod Idotea rotunda ta, mollusks such as the
limpets Siphonacmea oblongata and Col 1 isel la angusta.

In addition to the sea grasses, mangroves Are also found in the
tropics. These are ancient plants, which have adapted to life along the
sea shore. Mangrove stands are low (up to 5-10 m) evergreen groves,
rising from silty shores protected from the surf. The adaptation of the
mangroves to life in an amphibiotic medium on muddy, semiliquid silt
under conditions of physiologic dryness has been to develop stiltlike
roots which can survive in the air, pulpy leaves with watery stoma,
through which the excess of salts is excreted, reservoirs of fresh water
in old leaves and air-carying tissues in the fruit, allowing it to
float. Mangrove stands are common in the tropics and extend into the
subtropics from 35°N to 37°S. Nbst common are representatives of the
genera Avicennia , Rhizophora , Sonneratia , Laguncularia , Bruguiera and
Ceriops. Mangroves are the pioneers in the colonization of silty
estuaries by land plants and the advance of the shore into the sea.
Populating the brackish silts, suitable only for a very few halophiles,
they facilitate consolidation of the bed and its gradual transformation
to soil. In this way, they gradually create the prerequisites for the
formation of a tropical forest. The distribution of mangrove stands is

168

usually stratified. For example, in southern Florida Rhizophora is
located alony the lower boundary of the intertidal zone, then, closer to
tlie shore, Avicennia is seen. In the tropics, there Are as many as five
zones. The fauna of mangrove stands is not distinguished by great
variety, particularly the infauna, which is primarily a result of the
shortage of oxygen in the semiliquid ooze, ^bst characteristic are the
crabs Portunidae, Grapsidae, Ocypodidae, many of which construct
burrows, expelling a plug from the soil; the fish dre the Periophthalmus
and Boleophthalmus and the Gobiidae, and the gastropods Neritidae and
Littorinidae (particularly Li ttopinopsis) are present, as well as
oysters, and certain polychaetes. tony animals utilize the leaves and
trunks of the mangroves as substrates. The invertebrates are dominated
by detritophages, sestonophages (cirripedia and oysters) being
encountered only in the lower portion of the intertidal zone (Sasekumar,
1974).

In the temperate zone, in low places protected from the surf, salt
meadows or marshes are frequently formed. In contrast to mangrove
stands, marshes are not located in the intertidal zone, but above it,
and only certain halophilic plants frequently occupy the upper portion
of the littoral zone. The lower portion of the intertidal zone is
either populated with eel grass (Zostera) or contains no macrophytes at
all. This type of silty-sandy littoral below the marsh zone is referred
to as the tidal marsh. Mangrove stands and stands of halophilic plants
are different formations with different abiotic and physionomic
features. The only similarity is that the halophilic grasses and their
fauna and algoflora also consolidate the semiliquid bed and facilitate
its gradual conversion to soil. The pioneer of the higher plants in the
upper intertidal zone and in the sublittoral in temperate waters is
usually the halophyte Salicornia. The bonding of silt particles is
facilitated by the Corophium volutator amphipods and the mucus-
liberating algae which settle here. The halopohytes are followed by
multiannual plants such as Puccinella maritima, plus other salt-tolerant
species which settle on the substrate which they prepare:
Aster trifolium, Plantago maritima, Armeria maritima, etc.

Sandy, silted shoals, not subject to strong wave action, are
significantly more productive than open sandy beaches, which are poor in
detritus. Whereas the surf zones of sandy beaches are dominated by
euryphages, which can feed on fresh and decomposed plant and animal
residue, as well as living animals, silty-sandy shoals can support a
large number of detritophages which swallow the soil of the bed and sorb
detritus from the surface increases sharply. Silty shoals, completely
protected from the surf in some estuaries, lagoons and closed bays are
still more richly populated; in addition to the infauna, rich epifauna
develops, represented by the Littorinidae, Potamididae, mussels and
oysters, on which barnacles and other epifauna can develop and, in the
tropics, crabs, sea cucumbers and sea urchins.

The greatest biomass is that of the sestonophages--the mussels and
oysters, which frequently form continuous settlements, f'bst of the
remaining representatives of the epifauna collect detritus from the
surface of the bed. Various species living in the mass of the bed

159

burrow into it to various depths and thus utilize the nutrient resources
of the various layers of the bed.

Under subarctic conditions, and to some extent under the conditions
of the high boreal subzone, extensive, heavily silted spaces in the
estuarine intertidal zone are quite sparsely populated, with macrophytes
frequently absent, while the sparse macrofauna are represented primarily
by the amphipods and Mesidotea enotomon.

The biomass of the mussels and oyster banks (almost exclusively
animal) reaches several kilograms per iir. A significant biomass (up to
a few kilograms per m^) is also found in stands of marine grasses,
mostly plant biomass. In the remaining communities, the biomass is
significantly lower and reaches a few tens or hundreds of grams per m^,
both in the tropics and in the temperate zone.

160

2. The Communities of Coral Reefs. (Yu. I. Sorokin)

The biogeocenoses of coral reefs represent one of the most active
biologic systems in the world ocean, and in fact, on the planet as a
whole. The area occupied by coral reefs only in the Pacific Ocean is
comparable to the area of the continent of Australia. The biological
activity of the coral biogeocenoses, per unit area, is 20-100 times
greater than in the pelagic areas of the tropical zone of the oceans.
For example, the daily primary production of photosynthesis in the
coastal waters is 0.15-0.30 g C/mS whereas in coral communities of the
phytobenthos, periphyton and symbiotic zooxanthel lae, it is 5-20 g
C/mS The activity of the microflora, characterized by its destructive
activity and heterotrophic production in the coral biogeocenoses is 10-
20 times higher than in the surrounding oligotrophic tropical waters.

The processes of biogeochemical circulation of matter occur in
coral reef ecosystems much more intensively than in the surrounding
tropical waters and on the ocean floor. It is quite probable that it is
in the coral communities that microbial oxidation of the fraction of
organic matter resistant to sea water occurs (Sorokin, 1971a). Due to
the high productivity, optimal oxygen mode and high temperature of the
water in coral communities and in the regions of the surrounding shelf,
optimal conditions are created for the breeding and feeding of many
species of commercial animals.

Coral reef communities in and of themselves represent a classic
example of a biogeocenosis as a self-supporting community, which creates
its own physical substrate and chemical medium. At the same time, coral
biogeocenoses are distinguished from the surrounding oligotrophic waters
and exist basically on the energy of autochthonous primary production.
The system is organized so that the absolute concentration of nutrients
is maintained at a high level, in spite of an intensive exchange with
the surrounding oligotrophic waters of the ocean. The biological
mechanisms which maintain the reserves of nutrients and a high
productivity of the coral communities--conditions of an intensive
physical contact with the oligotrophic waters which pass over the reef--
represent an interesting problem. Its interpretation will doubtless be
of important significance in the creation of a theory of marine
aquaculture and will thereby assist in the solution of one of the key
problems of modern hydrobiology.

Primary production in coral communities is basically created by the
photosynthesis of hermatypic reef-forming organisms. The processes of
sedimentation of CaCOo and MgCOj on the reefs and, consequently, the
processes of formation of the reefs themselves and the sediments
surrounding them, are directly functionally related to the production
processes in the coral communities (Goreau et al., 1972). Therefore,
the study of the regularities of functioning and the production
processes of coral biogeocenoses provide the necessary basis for the
creation of the theory of growth of the reefs as the facies of
sedimentary rock of the earth's crust.

161

2.1 Reef-Bui1d1ng Organisms

A coral reef is a limestone structure capable of resisting wave
action, formed of hermatypic organisms on shallow platforms in the
tropical oceans and seas. A variety of benthic fauna and flora occupies
the limestone structures and accompanying porous limestone sediment of
corallogenic origin. The hermatypic organisms are both animals and
plants. Animal hermatypes include the reef-forming corals and certain
mollusks (Vermetidae, Tridacnidae) . In most reef builders, the active
deposition of the carbonates of calcium and magnesium is functionally
related to photosynthesis; hermatypic corals, as well as Tridacnidae,
carry many symbiotic algae, capable of photosynthesis, within their
tissues. Hermatypic plants in coral communities include the red and
green algae. Other groups with calcareous skeletons play a significant
role in the formation of the reef material : calcareous sponges, sea
urchins, polychaetes, ostracods, mollusks and foramini fera .

Usually 30-50 species of madrepore corals inhabit a coral reef,
primarily members of the families Agaricidae, Pocilloporidae,
Acroporidae, Poritidae, Faviidae, Asterocoenidae, Nbandrinidae,
Mussidae, as well as hydrocorals (family Mil leporidae) and octocorals
(family Hel ioporidae) . The plant hermatypes on reefs are represented by
30-40 species of calcareous algae: red (Li thotamnium, Peyssonel 1 ia ,
Porol ithon, Goniol i thon. Corall ina. Li thophyl lum, Sporol ithon, Tenarea)
and green algae (Halimeda, Penicillus, Udotea). The coral reef includes
a rocky calcareous structure and loose limestone sediment. The process
of formation of the rocky reef structure includes two successive stages,
performed by different species of hermatypes. First, the massive corals
( Favia , Siderastrea , Hydropora) or corals with massive, strong
appendages (Porites, Acropora , Pocil lopora) create the basic skeleton of
the growing portion of the reef. Certain calcareous algae also
participate in this process, forming massive outgrowths (Li thotamnium ,
Porol ithon) , which, however, play a secondary role (Goreau, Goreau,
1973).

The second phase in the formation of the rocky structure of the
reef consists of cementation of its skeletal basis and transformation
into a continuous, monolithic structure. This function is primarily
performed by the red calcareous algae (Lithotamnium, Porol ithon,
Peysonel 1 ia) , as well as the foraminifera , calcareous sponges
(Astrasclera) , mollusks (Tridacna, Vermetidae) and polychaetes
(Sabell idae) .

The calcareous algae are characterized by high rates of growth and
metabolism. The rate of formation of lime in these plants is much
higher than in corals. Therefore, it is these plants which form most of
the carbonaceous rock of the reef. The living corals usually cover only
a small portion of the rocky surface of the reef: not over 30-50% in
zones of active growth, and less than 5% on the reef plateau (reef
flat), occupying most of its surface. The loose calcareous sediment
(coral sand) covers most of the surface of the bottom of the lagoon.
The red Amphirhoa, Coral! ina, Goniol ithon) and green (Hal imeda)
calcareous algae are most significant in its formation. The Halimeda is
one of the primary agents involved in the formation of the lime material

162

of the bottom sediments in the reefs of the West Atlantic (Goreau,
Goreau, 1973). Another important source of material for the formation
of coral sand is the skeletons of dead corals, sea stars, sea urchins,
the shells of benthic mollusks, as well as the shells of ostracods,
foraminifera and pteropods, ground up by the surf.

2.2 Types of Coral Reefs, their Zonal ity. Growth and
Population with Flora and Fauna

Large reef structures can be subdivided into coastal, barrier and
atoll-type reefs. There are transitional forms between these basic
types as well. The development of any given type of reef depends on the
nature and tectonic mobility of the bottom on which it develops, as well
as the intensity of the arrival of terrigenous material from the land.
An important factor influencing the formation of the outlines of reef
structures is the fact that a most active growth of the corals creating
the skeletal basis of the reef occurs on the outer side of the reef, the
side directed toward the ocean. It is here that the optimal conditions
are created for the growth of coral (Yonge, 1953). On the inside of the
reef, the conditions are much worse for the growth of coral ; they
frequently die here. This factor leads to the formation of circular
atoll reefs where the growth of the corals is not limited by a
shorel ine.

Coastal, or fringing, reefs are usually formed on rocky plateaus of
small islands, with no significant terrigenous runoff, not subject to
constant tectonic downwarding. One characteristic feature of this type
of reef is that there is no lagoon. The reef plateau (reef flat) is
directly adjacent to the shoreline. An example of this type of reef is
the reef associated with the island of Titia (Fiji) (Fig. 1).

Barrier reefs are also formed on shallow coastline plateaus. They
differ from surrounding reefs in that there is a lagoon between the reef
flat and the shoreline. The lagoon is formed as a result of the death
of corals and cessation of their subsequent growth near the shore. The
growth of corals near the shore is depressed by the terrigenous runoff
and the decrease of the water in circulation. An example of a barrier
reef is the reef associated with the island of Tuvuta (Fiji) (Fig. 2).
The structures of barrier reefs achieve gigantic dimensions. The
largest of these is the Great Barrier Reef along the east coast of
Australia. It is an entire system of reefs extending about 2000 km in
length, with a total area of some 250,000 km . In contrast to most
other reefs, where the main mass of the lime material is created by
calcareous algae, the Great Barrier Reef was constructed by corals, the
algae being of secondary significance. The thickness of the reef
limestone, according to drilling information, is 300-700 m (Ladd,
1969). The second largest barrier reef, over 700 km in length, is
located off the north and northeast coasts of the island of New
Caledonia. The third is considered to be the barrier reef off the north
coast of the Fiji Islands. Its length reaches 400 km. The barrier off
the coast of Arabia in the Red Sea is also worthy of mention in any
discussion of large barrier reefs.

163

The circular reefs of atolls develop on the peaks of submerged
mountains or guyots, rising nearly to the surface of the water. The
growth of the reef in this case is not limited in space, and its
circular form is a result of the more favorable conditions for the
growth of coral on the outside of the reef. Inside the reef is a sandy
lagoon with the residue of a broken rocky base, on which sandy islands
usually develop, or underwater pinnacle banks. Inside the lagoon,
around the islands and on the remainder of the reef flat, the coral
organisms develop in groups, forming so-called "spot reefs."

The structure of a circular reef is shown in Fig. 3, where we see
the plan and cross section of the reef of Conflict Atoll (New Guinea).
The structure of this atoll reef is similar to that of the barrier reef,
except that there are no large islands within the lagoons of the
atoll. The largest atolls are Kwajalein Atoll (Marshall Islands) and
Suvadiva (Mai dive Islands). Their areas approach 2500 km .

The zonal ity of the structure of the reefs has been studied in
detail by T. Goreau. The plan which he has suggested rather completely
reflects the zonal ity of the distribution of the primary biotopes as
well. The zones distinguished by T. Goreau and his colleagues (Goreau
et al., 1972; Goreau, Goreau, 1973) are shown in the cross sections of
the primary types of reefs (see Figs. 1-3). They are most completely
represented in the barrier reef, so we shall use this plan to present
our detailed description of the individual zones and their corresponding
biotopes.

The I (inshore) zone is the shore zone, depth less than 1 m. This
is the littoral beach. Its population is exposed to the influence of
drying out during low tides and to the terrigenous runoffs from the
land, leading to silting of the bottom. If silting is severe, mangroves
develop in the inshore zone (see III. 1).

Frequently, the inshore zone consists of rocky beds--crust rock or
the remainders of an old reef, broken up with cracks. Here we find a
rich fauna of mollusks (the gastropods Tectarius, Littorina, Nerita,
Thais, Vasum, Conus, Cymatium, Purperita, Cypraea, Col umbel la, chitons),
hermit crabs (Coenobita, Paguridae), crabs, sea urchins (Diadema,
Echinometra, Eucidaris) and the Ophiuroidea (Macrophiothrix) .

The main source of nutrition of the fauna is the plant fouling of
the rocks (periphytons) and plant material thrown out on the beach by
the waves. The biomass of the fauna sometimes is quite significant.
For example, off the coast of Florida, the biomass of chitons alone in
the inshore zone of the reef at the water line is as great as 40 g/m^
(Glynn, 1973).

The L (lagoon) zone, depth 2-20 m is present in all barrier reefs
and atolls. The lagoons of barrier reefs usually are subjected to the
influence of terrigenous runoff and differ from the lagoons of atolls in
their more eutrophic conditions the predominance in them of hetero-
trophic processes. The bottom of the lagoon of a barrier reef is
frequently silted. Silting of the lagoon greatly influences the
composition of its fauna (Goreau, Yonge, 1968). Upon silting, and under

164

/Om

Fig. 1. Diagram of profile and zonality of fringing reef of the Titia
Island (Fiji). 1, Sand; 2, Rocky reefflat; 3, Dead coral and fragmentary
material; 4, Living coral. For symbols of zones, see text (Sorokin, 1975),

Fig. 2. Diagram of profile and zonality of barrier reef at the Tuvuta
Island (Fiji) (Sorokin, 1975). Symbols same as Fig. 1.

Fig. 3. Diagram of profile and zonality of upwind reef of the Conflict
Atoll (Louisiad Archipelago, New Guinea) (Sorokin, 1975). Symbols same
as Fig. 1 .

165

the influence of pollution, reduced sediments may appear in the lagoon,
containing sulfides and hydrogen sulfide (Sorokin, 1971b). The bottom
of the lagoon in atolls is covered with coral sand. If the movement of
the water is low, it is inhabited by macrophytes (Zostera , Thalassia ,
Halophila , Halodul e, Syringodium , Enhal us) and psammophilic green
calcareous algae (Halimeda, Amphirhoa, Avrainvillea) . The sand on the
bottom of the lagoon also contains a rich microflora and phytobenthos.
They form the diet of the gastropod fauna living here (Strombus ,
Terebra , Cymatium, Cerithiidae, Leucozonia , Oceanebra , Astraea , Conus ,
Mitra, 01 iva. Morula , Hyal ina , Tegula, Turridae) . Among the
psammophilic fauna, the Ascidia, Echinodermata (the sea stars Linckia,
Culci ta, the urchins Diadema and particularly the Stichopus, Holothuria
and Ophiodesma). The Holothuria sometimes form massive accumulations,
in which their biomass per m of bottom surface reaches 1 kg or more.
These accumulations are formed, e.g., by Ophiodesma spectabili^ in the
lagoon of Oahu Island (over 10 indiv./m^, biomass about 3 kg/m^) or
Holothuria difficil is in the lagoon of Eniwetak Atoll (over 100
indiv./m^, biomass about 10 kg/m^) (Bakus, 1973, and our own
observations). The sand of the lagoon is inhabited by a mass of
polychaetes (Heteroptera, Sabellidae), as well as varied myobenthos
(foramini fera , ostracods, micromol 1 usks) and microbenthos
(microphytobenthos and bacteria). An abundant population of the sandy
soils of the lagoon gives them high trophic value. The fauna and
detritus which can be extracted from the sand form the diet of many
benthophagous fish.

Among the corals in the lagoon there Are almost always forms which
prefer higher levels of illumination (Porites, Ocul ina, Favia ,
Siderastrea , fentipora , Pavona , branched forms of Acropora and
Millepora) . Conditions for growth of corals in lagoons are frequently
unfavorable due to significant water turbidity and a low rate of water
exchange. If this is the case, a mass of dead coral and fragmentary
material accumulates on the floor of the lagoon. The living coral grows
in the lagoon in certain areas, forming "patch reefs," which rise over
the bottom of the lagoon in the forms of hills or ridges covered with
living coral and corallines.

The R (rear) zone is situated at the internal edge of the reef,
depth 1-3 m. This is the re^r slope of the reef plateau. It is usually
covered with rubble carried down from the reef flat, and is crossed by a
network of channels, the bottom of which is covered with sand and
clastic materials. Zone R is characterized by significant turbulence
from surf waves, which roll over the edges of the reef, as well as tidal
currents, and also by a high level of illumination. This creates an
optimal condition for the growth of corals, calcareous algae and
macrophytes, which inhabit the remainders of the plateau and form
independent, broad colonies. The dominant species of corals here are
usually the branching forms (Porites compressa, Acropora, Seriatopora,
Millepora) , as well as the fan-shaped and massive forms (Diploria ,
^bntrastrea, Favia, Favites , Hydropora, Dichocoenia, Acropora cuneata,
itorrUpora^, Porites lobata, P_. lutea, _P. asteroidesT. On the bottom of
the channels between the patch reefs and beneath the lip of the plateau,
we frequently see the solitary corals, Fungia. Soft corals
(Alcyonaria) , macroalgae ( Chlorodesmium , Thalassia, Padina, Sargassum,

166

TurbindrJa) and calcareous algae (Porol ithon, Jania , Caulerpa) occupy a
significant position on the reefs.

The R zone, as a rule, is inhabited by a varied benthic fauna.
According to averaged data (Glynn, 1973) on the reefs in the Caribbean
Sea in this zone the wet, lime-free biomass of animal matter of the

benthos is about 4 kg/m (Table 3). If we include the skeletal mass
the biomass reaches 120 kg/m (Colikov et al . , 1972). This is near the
maximum possible biomass of the benthos in eutrophic biotopes.

Table 3. Mean biomass of benthic fauna and flora on reefs of the
Caribbean basin in the R zone with predominance of the coral Porites
(Glynn, 1973).

Dry matter, including Wet biomass of
Group of organisms skeletons living matter

Madreporaria 12,022 2,855

Echinodermata 263 526

Foraminifera 136 18

Mollusca 59 100

Crustacea 40 149

Sponges 12 58

Polychaeta 7 32

Fish 6 36

Zoantharid and colonial sea anemones 1 4

Zoobenthos, total 12,546 3,780

including filter feeders - 3,000

Massive macroalgae 1,022 325

The fauna, in addition to coral, includes hydroids (Pennaria) . The
gastropods are numerous here, inhabiting the loose sediment between
reefs. These include primarily the same genera as are found in the
sandy lagoons, plus some others (Terebra, Cerithium, Rhinoclavis,
Pterygia) . Among the large gastropods which inhabit the clastic
material and feed on the periphyton, Lambis, Strombus and Cassis
predominate. On hard surfaces and in clefts in the reef we find
Fissurella, Astraea, flirex. Turbo, Cypraea, Trochus, Lunella, Bursa,
Ctena, Chione, Diplodonta , Anodontia), sponges ( TeThya ) , A"?c i d i a , crabs,
pencil sea urchins (Cidaridae), Ophiuroidea, starfishes (Culcita) ,
Holothuria (Holothuria. Stichopus), Polychaeta (Serpulidae,
Dendrostoma). As to biomass and variety, the benthic population of this
zone is among the richest biotopes on the reef.

The Fl (reef flat) zone is the rocky plateau of the reef, depth
0.5-1 m. The shallow reef flat may extend for up to 100 m or more. It
is subjected to strong surf action. Individual shoal sections of the
reef flat and the limestone rocks located on their surface (so-called
"niggerheads" ) extend above the water surface at low tide. The flat is
cut through by channels and cracks, through which the loose bottom

167

sediments and clastic niaterial is transported. The flat is a zone of
active calcification. In most reefs, the primary role in this
calcification process is played by the calcareous algae (Neogoniol ithon ,
Porol ithon, Li thotamnium) . In some reefs, they construct a purely algal
limestone reef flat (Kornicker, Boyd, 1962; Glynn, 1973). The growth of
the limestone mass of the reef flat is accomplished by the algae and
also by polychaetes (Dendrostomidae, Sabellidae), which construct the
limestone tubules. The entire porous surface of the reef flat is
covered with a dense cover of periphyton, consisting of filamentous
macrophytes, filamentous blue-green algae and diatoms. Stands of
macrophytes with short, strong thalli are also seen (Turbinaria ,
Laurencia, Chnoospora , Hydroclarthus, Sargassum, Padina), plus large
colonies of soft coral s~TZoantus ) 7~col onial sea anemones (Palythoa) .
various individual sea anemones, Ascidia and sponges. Living coral
(Acropora, Siderastrea , Pocil lopora , fentastrea , Pi ploria , Mil lepora ,
Favia, Coeloria, Dicoenia , Leptastrea) grow on the surface of the reef
flat sparsely in the form of massive crusts or low colonies. The rocky
plateau and the "niggerheads" are populated by Gastropoda (Li ttorina ,
Neri ta , Trochus , Gonus , f-tnetaria , Cypraea , Murex , Bursa , Turbo,
Lunel la , Astraea , Hal iotis, Mancinella), various crabs, stars,
Ophiuroidea, Polychaeta ( Capital 1 idae, Nereidae, Phyl lodocidae) . The
periphyton and rich fauna serve as food for many fish which come to feed
on the reef flat during high tide.

The Br (breaker) zone is the frontal edge of the reef where the
waves break, 1-2 m deep. The population of corals living here is
constantly subjected to the powerful mechanical effects of the surf.
Their growth is determined by their strength. If the reef is in the
path of tropical cyclones, the tremendous waves which arise during these
storms may crush off all living coral on the outer edge of the reef down
to a depth of 5-8 m (Goreau, 1959; Glynn, 1973; Stoddart, 1974). The
underlying zones (Mix, But, Fr) , after the cyclone passes, Are buried in
fragments and colonies of broken coral (personal observation of the
author on the Lau Islands). Strong typhoons sometimes break down even
the rocky reef plateau or bury it in clastic material, as a result of
which new islands arise. This occurred at Funafurti Atoll (Ellis
Islands) in 1971.

In spite of the strong mechanical action of the surf, conditions
for the growth of coral here Are optimal, due to the high turbulence and
good illumination. Therefore, a dense population of young coral usually
arises in the breaker zone, with strong, massive colonies withstanding
the waves. Such are the colonies of coral Acropora (Acropora palmata,
_A. cuneata , _A. corumbosa) , as well as Stylophora pistillata,
Millepora platyphilla, H. complanata , Mjntipora hoffmeisteri ,
Porites lutea, P_. asteroides, Pocillopora damicornis, Diploria strigosa,
and Favia fragum. The calcareous algae Li thothamnium and Porol ithon,
which form massive colonies in the breaker zone, are very significant in
strengthening this zone. Among the benthic fauna, forms which live in
cracks in the rocky base and in the colonies of dead corals are
predominantly ascidians, sponges, crabs, and various polychaetes.

f-b (moat) zone--3-5 m deep. This zone has the shape of a long
moat, along the edge of the breaker zone. The moat is formed as a

168

result of suppression of tlie growth of corals in the area where the
loose sediment and clastic material, carried away from the reef flat by
the surf and tide, drifts down. Since active growth of coral proceeds
lower down the slope, in the Mix zone, a moat is formed between the Br
and Mix zones. Its bottom is covered with sand and a mass of fragments
of coral, among which are living solitary coral s/ Fungia. The clastic
material is densely populated with periphyton, which is eaten by the
large mollusks (Lambis, Bursa , Murex, Turbo, Trochus) .

The main mass of the macrobenthos consists of infauna, which
inhabits the colonies and large lumps of dead corals accumulated on the
bottom. Here dre masses of polychaetes, decapods, amphipods, isopods,
ol igochaetes, sipunculides and Ophiuroidea.

The Mix (mixed) zone, 4-8 m deep. It occupies the slope, with
rather abundant growth of corals, which extend to the next zone.

The Bu (buttress) zone, 8-20 m deep. This is one of the most
important and rapidly growing elements of the reef. Here the most
intensive growth of corals occurs and the greatest taxonomic variety is
seen (Table 4). The growth of corals occurs in strips, located
perpendicular to the edge of the reef. It is divided by slots, through

Table 4. Distribution of massive species of coral over an area of 90 m
in the main zones of the frontal part of reef at Heron Island, Great
Barrier Reef (Grassle, 1073).

Zone Species cm

Total dred of colonies,
^•10-^ in an area of 90 m'^

Fl Acropora cuneata 14.0

9.7

A. squamosa
Porites andrewsi

Pocil lopora

damicornis

Acropora corumbosa

A. cuneata
Millepora pi

atyphyl la

Pocillopora

damicornis

Acropora formosa

Montipora sp.
Acropora hyacinthus

Seriatopora

hystrix

Pocil lopora

damicornis

3.4
2.6

Br Acropora corumbosa 5.5

4.5
1.6
1.4

Mix + FR Acropora formosa 196.9

65.7

36.1

5.3

2.2

which the sediment and clastic material mo>'e. As a result of this
localization of the active growth of coral, rows of large, limestone
humps are formed. Their surfaces are densely covered with corals, which

169

find optimal conditions here for' their growth: d high degree of water
turbulence, sufficient illumination, intensive development of plankton,
consuming the organic matter which flows down from the reef. The large
fan-shaped and branched forms of coral predominate: Agaricia, Mussa,
Fa V i a , Acropora , Ser i a to po ra , Madracis , Pterogorgia , Gorgonaria bloom
(Ell isella , Nicella, Viminel la, Pseudopterogorgia, Plexaura) along with
soft coral s "(Sclerophytum) , which compete wittt the corals for the solid
substrate and frequently form continuous growths. The Bu zone is rich
in sponges (Ircina , Kycale, Agelas , Verongia) , some of which reach
almost 1 meter in diameter. The fauna includes crinoids (Nemataster) ,
boring sponges ( CI ionidae) and mollusks (Li thophaga , Fungiclava) , which
make paths through the living coral. An unusually rich fauna inhabits
the dead colonies of coral and the rocky base. In one such colony,
brought up from a depth of 15 m, some 8000 individual organisms of
macrobenthos of 50 species were found (f'tCloskey, 1970).

The PR (fore-reef) zone, depth 20-40 m. This zone occupies a steep
slope, on which a kind of cliff (so-called "sill-reef") is sometimes
forming, which consists primarily of the massive corals Montastrea,
Agaricia and Madracis. This zone is characterized by a rapid growth of
corals, which form a large colony (Astrangia , Agaricia, f-tonti pora ,
Millepora, Mussa). Calcareous algae (Halimeda, Peyssonellia) develop
intensively here as well as a rich zoobenthos, which includes various
attached forms (polychaetes , sea lilies, Bryozoa, hydroids,
gorgonarians, ascidians, colonial sea anemones, soft corals). A
significant role in the deposition of lime in this zone is played by the
calcareous sponges (Sclerospongia) , which reach a significant size and
d.re encountered in large quantity, particularly on the walls of the
canyons and caverns (Goreau, Goreau, 1973).

The discovery of the abundant development of coral communities at
significant depths at the foot of a reef (Goreau, 1959) was one of the
most important achievements of Goreau in the study of coral
ecosystems. His observations on the structure of the deep zones of the
various reefs have shown that the structural form of the reef is
determined not by processes of erosion, but by the localization of the
growth of corals. The localization of the coral growth, in turn, is
regulated to a significant extent by the complex movement of the bottom
sediment and clastic material over the profile of the reef, since in
sediment covered areas of the reef, over which it flows, colonies of
massive corals cannot settle and develop, creating the buttresses of the
reef. Their surface can be inhabited only by solitary corals ( Fungia) ,
which lie freely on the ground, or by highly branched forms (certain
Acropora). As the corals grow, the troughs filled with reef sediment
Are converted into deep canyons with steep walls. These canyons are
gradually covered over by massive colonies of coral growing on their
side walls, and converted into caverns. In the Br, Mix and Bu zones,
caverns are normal elements of the external side of a reef.

Individual species of organisms are rather clearly restricted to
specific zones of the reef. However, if we analyze the species
composition of the madrepore corals and algae in various zones of the
Jamaica and Great Barrier Reefs (Goreau, Goreau, 1973; Grassle, 1973),
we can see that certain species of coral inhabit all zones of the

170

reef. These opportunistic" species include, for example,
Pocillopora damicornis , Porites asteroides, fentrastrea annularis,
Acropora cervicornis, Stylopora pistil lata. There are species (e.g.,
Porites porites) which populate the shoals (zones L and R) and the
deeper zones of the outer slope (Bu, FR), but are practically absent in
the surf zones on the rocky plateau ( Fl , Br, ^b, Mix). Finally, a
number of species occupy the slope biotopes (Bu, FR, FRS) but are not
encountered at depths of less than 20 m (Agaricia grahami ,
Kddracis mirabil is , Nycetophyl la reesi , Acropora hyacinthus ,
Seriatopora hystrix). The "opportunistic" forms, encountered in all
zones of the reef, characteristically are able to change the form of
their colonies, depending on conditions of illumination and
turbulence: branched colonies in the lagoon, and massive colonies on
the reef flat.

2.3 Ecological and Physiological Features of Reef-Forming Corals
and Factors Influencing their Growth and Distribution

f'ciny fundamental peculiarities of the coral communities result from
the ecological-physiological properties of the hermatypic corals
themselves. They include: the diversity of ways of feeding of corals,
including photosynthesis, the coupling of the process of calcification
with photosynthesis and the antagonistic interactions between some coral
species.

The diversity of ways of feeding of madrepore corals makes them, in
a certain sense, a unique set of hydrobionts. They possess practically
all known types of feeding behavior peculiar to aquatic invertebrates
and have the specific morphologic structures and enzyme mechanisms for
this purpose. Because of the presence of symbiotic algae in the tissues
of their polyps they are capable of autotrophic nutrition, like green
plants. Their growth, like the growth of plants, depends on light also
because the precipitation of CdC03 and MgCOo from the water by them is
directly dependent upon illumination (Muscatine, Cernichiari, 1969;
Goreau, 1963; D. J. Barnes, 1973). The well-developed ciliar epitheliu
and the streamlike movement of mucus along the tentacles of the polyps
allow the corals to obtain nutrition from the detritus and micro-
organisms suspended in the water. The operation of the ciliate
apparatus and the presence of the required enzymes gives them the
ability to utilize organic matter dissolved in the water. Finally, the
polyps are capable of predatory feeding. The polyps catch their prey
using their stinging cells, then digest the prey inside their gastral
cavity or outside of the polyp's body by means of their mesenterial
filaments. These combined ways of feeding eliminate the basic factor
which limits the development of life in the poor surface tropical waters
of the ocean: the shortage of nutrients such as nitrogen and
phosphorus. Actually, due to their heterotrophic nutrition, the corals
can utilize the organic sources of nutrients (Sorokin, 1973a). The
processes of autotrophic production and heterotrophic decomposition of
organic matter, combined in a single organism, provide a closed cycle of
nutrients with minimum losses into the environment (Johannes et al . ,
1970). This is not feasible for heterotrophs , the metabolism of which
occurs only under conditions including liberation of nitrogen (in the
form of urea) and phosphorus (in the form of inorganic phosphate) into

171

urn

the environment. These products of heterotrophic metabolism are
utilized in the autotrophic biosynthesis of the zooxanthellae, without
leaving the organism of the polyps. It has been established that
hermatypic corals, having zooxanthellae, excrete much less inorganic
phosphate per unit of biomass as compared with hermatypes, which do not
have zooxanthellae, or with other marine animals (Yonge, Nicholls, 1931;
Pomeroy et al . , 1974).

An intensive photosynthesis (Table 5) is inherent for the corals,
in spite of the fact that the biomass of the zooxanthellae represents
only a few percent of the biomass of the polyps (Table 6). The mean
intensity of photosynthesis of madrepore corals is 0.2-0.3 mg C/g of dry
matter of the colony, or about 5 mg C/g of organic matter of the polyps
per day. The production of photosynthesis usually exceeds the losses of
polyps to metabolism by 1.5-3. Therefore, for most corals inhabiting
areas with optimal conditions of illumination, energy losses can be
completely compensated for by photosynthesis. When this occurs, about
half of the organic matter synthesized by the zooxanthellae is found
within a few hours as part of the tissue of the polyps (Muscatine, 1967,
1973i Von Holt, Von Holt, 1968). Such an intensive autotrophic
production of organic matter is achieved due to a high intensity of
photosynthesis of the zooxanthellae, the daily P/B coefficient of which
is about 2 to 5.

In addition to the production of organic matter, the functioning of
the zooxanthellae enhances the process of calcification in the
construction of the skeleton of hermatypic corals, and so of the growth
of the reef itself. With the use of isotope Ca, it has been shown that
the process of accumulation of calcite in the skeleton of the corals
depends directly upon the intensity of the light and the presence of
zooxanthellae (Goreau, Goreau, 1960). The addition of specific
photosynthesis inhibitors to the water inhibits also the process of
precipitation of calcium carbonate in the skeleton of the corals.

The capability of corals to feed on microplankton has been proven
experimentally, using phytoplankton and bacteria labeled with C-"-^ or S-^^
(DiSalvo, 1973; Sorokin, 1973e). This sedimentation mode of feeding of
corals is based on trapping of the nutritious particles (bacteria,
algae, protozoa) by the mucous surface of the body of the polyp and
their transfer by the action of cilia to the mouth (Yonge, 1968;
Muscatine, 1973). Apparently, the coenosarc (the tissues covering the
surface of a colony between polyps) also may participate in the process
of sedimentation feeding, which may significantly increase the intensity
of sedimentation feeding (Goreau, 1959). According to the observations
of Goreau, the nutritious particles which precipitate onto the mucous
surface are transferred toward the polyps by the movement of the mucus.

Determinations of the intensity of the sedimentation way of
heterotrophic feeding of massive species of coral (Pocil lopora , Pori tes ,
Fungia, Montipora), using bacteria labeled with C-^^ as the food, have
shown that this method of nutrition can compensate for up to 10% of the
daily losses in metabolism (Fig. 4). The phytoplankton is consumed and
assimilated by the polyps much more poorly than the bacteria, since the
polyps are not capable of digesting plant cells (Yonge, 1930).

172

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174

In evaluating a relatively low rate of sedimentation and predatory
feeding by coral (Johannes et al., 1970), we must consider that coral
receives the bulk of the energetic material it needs by photosynthesis
of zooxanthellae. The heterotrophic feeding serves corals not only as a
source of energy, but also as a way of supplying them with necessary
nutrient salts, vitamins, trace elements, as well as with some essential
amino acids which are not produced by the zooxanthellae.

The digestive organs used for predatory feeding are the mesenterial
filaments which line the edges of the septa in the intestinal cavity.
These filaments Are mobile and may extend outside the oral aperture by a
distance of up to 10 cm, causing predigestion of large prey items
outside the intestinal cavity. They literally weave around the food and
digest it with exoenzymes.

Experiments have demonstrated that when there is a significant
concentration of zooplankton, corals with large polyps (such as
^bntastrea) are capable of completely satisfying their requirements for
food by predatory feeding (Coles, 1969; Porter, 1974). However,
usually, the concentration of zooplankton over reefs is so low that it
cannot satisfy the energy demands of the coral (Johannes et al., 1970;
Johannes, 1974). Predatory feeding of coral is probably increased
during the period of massive development of invertebrate larvae
(veligers, trochophores, echiniopl uteus larvae, etc.). Calculations of
the difference in concentration of plankton in the lagoon and in the
surrounding atoll waters have shown that the consumption of plankton by
the coral community can cover about 5-10% of the energy expended in
metabolism (Johannes et al., 1970; Glynn, 1973).

Furthermore, coral is capable of feeding effectively on organic
matter dissolved in the water at concentrations near the natural
concentration: 1-2 mg c/Z (Stephens, 1960). With this concentration
glucose or protein hydrolysate, the corals in our experiments
assimilated the dissolved organic matter in quantities sufficient to
cover 15% of the daily expenditure for metabolism (Sorokin, 1973a).
About half of the labeled organic matter consumed by the coral is
included in the composition of the matter of the polyps (Lewis, Smith,
1971).

Experiments on Pocil lopora have shown that the rate of consumption
of one labeled amino acid at a concentration of 0.1 mg C/ i is not
reduced when other nonlabeled amino acids are added at 100 times greater
concentration (Sorokin, 1977). Obviously, the corals have a mechanism
for enzymatic (permease) transport of dissolved organic matter into
their cells. Effective consumption of organic matter is provided by the
large surface dreA in contact with the water due to the ciliated
epithelium and mesenterial filaments. The significance of this way of
feeding of corals under natural conditions requires further
clarification.

The phenomenon of interspecific antagonism and aggressiveness of
coral species has considerable value in the population ecology of coral
communities (Lang, 1973). An entire hierarchy of such relationships has
been found between various species of coral. When two species of

175

Fig. 4. Intensity of assimilation (A, ,ig
C/g 'day) of food labeled with C-'-^ by coral
with various food concentrations (K, ug
C/liter); 1, Dissolved organic matter
(algae protein hydrolysate) ; 2, Bacterial
plankton; D, assimilated food, % of
expenditure for metabolism (with correction
for loss of C-'-^ during time of experiment);
Ki and K2--probable natural concentrations
of bacteria and dissolved organic matter in
the water around the coral reefs.

/^/^ zoo 300 ¥00 m/c

coral come in contact, the polyps of the more aggressive ("stronger") sptvies
extend their mesenterial filaments toward the "weaker" species, enclose and
digest its polyps. Nbst aggressive are the massive, slowly growing species of
Favia, "weakest" are the species of Agaricia, which live at considerable depth
and, apparently, do not experience great competition from the other
madreporaria. Acropora occupy an intermediate position.

The growth rate of hermatypic corals depends to a great extent on the
level of illumination at the point of attachment of the colony. In the dark,
the hermatypic corals die within a few months. Under optimal growth
conditions, in two or three years, coral colonies can grow to a diameter of
10-20 cm, doubling their size each year. The mean age of colonies in the
zones of active growth (FL, Br, But) is about 5 years, the maximum age--up to
140 years. The mortality of young colonies is great--20-40% within 3 years
(Connell, 1973). In spite of the high rate of growth of young corals,
replacement of their populations after passage of a destructive typhoon is
quite slow. The additional stage of settlement of the damaged frontal zone
with corals and the succession of communities which follows extend over a
period of 3-5 years (Stoddart, 1962, 1974; Glynn, 1973), while full
restoration requires over 30 years.

The composition and populatio
such natural enemies as the boring
(Pang, 1973). They drill holes in
resistance to the surf. Many reef
polychaeta, gastropoda, fish) feed
their outer layer. The most dange
Acanthaster planci . Over the last
animal on certain reefs in the Ind
observed (Endean, 1973; Connell, 1
stars are usually found quite rare
km"^. Following massive breeding,
several individuals per 10 m^. Mo
destroy up to 90% of the corals,
after they pass.

n of corals i
sponges Clio

to the living

animals (sea

on the coral

rous predator

10-15 years,

ian and Weste

973). These

ly on the ree

their populat

ving over the

The coral req

s significantly influenced by
ne and the mollusks Ithophaga
coral and decrease its
urchins, sea stars, crabs,
, eating the polyps or removing
for the coral is the starfish
population explosions of this
rn Pacific Oceans have been
large--mean diameter 30 cm--
fs, a few individuals per
ion density increases to
reef in compact groups, they
uires many years to recover

176

2.4 Perlphyton, Phytobenthos , Primary Production and Microflora
In Reef Blotopes

When we speak of the algoflora of a reef and Its production, we generally
mean macrophytes and calcareous algae. However, most of the primary
production In coral biogeocenoses is created, apparently, not by the
macrophytes, but rather by the periphyton and microphytobenthos. The
perlphyton abundantly overgrows all rocky surfaces of the reef flat, the
porosity of the calcareous material of the flat significantly increasing the
Area and mass of the overgrowth. The perlphyton develops particularly
intensively on colonies of dead coral and their fragments, fbst of the
perlphyton consists of filamentous and mucous forms of bluegreen algae and
diatoms (Osterobium, Calotrix, Microcoleus, Shizotrix, Rivularia, Ni tzschia ,
Navlcula, Cymbella). In addition to these, we also see certain macrophytes
with short, filamentous thalloms (dwarf forms of Laurencia, Sargassum,
Polysiphonia and Gelidella). The biomass of algae in the periphyton is 2-5
mg/g (Sorokin, 1973d). The photosynthesis of the periphyton over the dead
corals amounts to 100-500 iig C/g dry weight of dead colony per day (Table 7).

The photosynthesis of the periphyton on dead corals expressed as dry
weight of the colony, averages close to that on living coral of the same
species and configuration. The daily production of photosynthesis of
perlphyton over dead corals is about 3% of the total content of organic
matter, averaging 3-5 g C/m'^. The production is equally intensive In
periphyton over the clastic material and over the reef flat rocks (Tables 5,
7). The production of macrophytes on the Great Barrier Reef averages about
0.3 g C/m^ per day (Grassle, 1973).

The respiration of the periphytonic community is also rather intensive,
50-100% of the production by its photosynthesis. The same relationship
between photosynthesis and respiration was also found for living corals
(Tables 5, 6). Thus, the periphyton community, like the living corals, fully
supplies itself with energy by photosynthesis, in spite of a significant
quantity of heterotrophic organisms in it. It is quite probable that some
closed cycles of nutrients exist in the perlphyton community, since the
primary producers and reducers are combined into single agglomerates by mucus
excreted by the algae. This, in particular, may explain the richness of the
periphyton, even on the outer side of the reef, which is washed with water
that is practically devoid of the inorganic forms of nutrients.

The coral sand which occupies most of the area of the atolls and of
certain barrier reefs Is also abundantly populated with microscopic algae.
The sand particles are fragments of coral skeletons or coralline algae of the
shells of foramlnifera and ostracods. They are covered with a mucous film
containing algae and bacteria. The wet biomass of phytobenthos In the sands,
based on the results of direct measurements (Sorokin, 1973d, e) , was 0.5-1
mg/g, based on calculations of the intensity of photosynthesis, about 2
mg/g. Measurements of the photosynthesis of the phytobenthos by the
radiocarbon and oxygen methods (Sorokin, 1971b, 1973d, e, 1975a) have yielded
similar values: 30-60 pg C/g per day. The thickness of the photosynthesis
layer in the coral sand on Funafuti Atoll is 3 cm, but it decreases rapidly in
the first centimeter of sand. Calculation of the production by photosynthesis
of the phytobenthos in the sand yields a value of about 1 g C/m , which is 3-5
times higher than the primary production of photosynthesis by phytopl ankton in
the 100-meter euphotic layer of tropical waters.

177

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178

The intensity of respiration of the community of microorganisms
populating the coral sands of an unpolluted living reef is, on the
average, comparable to the magnitude of photosynthesis (Table 7).
Respiration is significantly greater than photosynthesis in the sands
deposited directly beneath the living coral, and in the loose sediment
of a polluted reef (Sorokin, 1973e). Each day, photosynthesis causes
the renewal of about 1% of the total organic carbon in the sand.

The intensity of photosynthesis of the coral community is 3-10 g
C/m per day (Sargent, Austin, 1953; Odum, Odum, 1955; Odum et al . ,
1959; Kohn, Helfrich, 1957, Kinsey, Kinsey, 1967). This is 30-50 times
higher than the production of phytoplankton in the column of
oligotrophic waters surrounding the reef.

The most important component in the periyhytonic communities of the
reef is bacteria. Their population is I-5'IO cl/g in the sand, 3-5*10
in periphyton, and up to lO'lO in regenerative sediment (Table 7).
Such a high population of bacteria can be found only in the bottom
sediments of eutrophic lakes. The number of bacteria in the
regenerative sediment of the polluted reef in Kaneohe Bay, Hawaii, was
close to the number in the active silt of sewage purification plants
(Sorokin, 1973e).

f'bst of the microflora of the periphytonic overgrowth of solid
substrates (dead coral, the rocky reef flat) consist of mobile
filamentous flexibacteria such as Leucotrix, as well as catenulate
bacteria such as Cladotrix and Crenotrix, which usually develop in
bodies of water rich in organic matter.

The biomass of bacteria in the periphyton and in bottom sediments
of the coral reefs varies within 50-500 ug C/g, or about 5 g/£ of wet
biomass (2-3% of the total organic matter of the substrate). The
production of microflora in the bottom sediments and periphyton is 20-
200 pg C/g per day, the P/B ratio averages 0.2-0.7. Thus, the matter of
the benthic microflora of the coral reef is totally renewed in 2-5 days.

2.5 Structure and Productivity of the Planktonic Communities over
Coral Reefs

The plankton of reefs is relatively much poorer than the benthos,
its biomass and production being many times lower than that of the
benthic communities. Thus it mibht be concluded that the plankton is
insignificant in the energetics and functioning of the ecosystem of the
coral reef. However, this conclusion would be erroneous, because the
predominant benthic fauna of the reef are fil ter- feeders and sediment
feeders which consume the plankton (Glynn, 1973). The underevaluation
of the significance of the plankton is partially due to a failure to
consider the main producing and nutritive component of the plankton in
coral communities--the bacterioplankton. The plankton and the organic
matter dissolved and suspended are the key links by means of which the
individual biotopes of the reef Are energetically connected, thus
forming the unified coral reef ecosystem. This energetic connection is
achieved both by direct transfer of the larval planktonic stages, which
serve as a source of nutrition for the coral, and by transfer of

179

dissolved or aggregated organic matter, liberated by the coral and

algoflora, detritus, bacteria, algae, protozoa which is washed out into

the water from the coral sand, and periphyton of the shallow zones of
the reef by the action of the waves and currents.

The wet biomass of phytoplankton over the reef averages 20-100
mg/m'^; the production averages 10-30 mg C/m'^ (Sorokin, 1971c, 1973b).
It is significantly higher on reefs located in eutrophic regions, for
example. New Guinea or Puerto Rico (Glynn, 1973). The lowest biomass
and production of phytoplankton are reported for reefs located in
oligotrophic waters of the ocean (Table 8). The seasonal nature of
phytoplankton development is of great significance. During periods of
maximum development, the biomass and production of phytoplankton may
increase by an order of magnitude in comparison to the mean annual
values (Sournia, 1969). Periods of massive appearance and precipitation
of benthos larvae in the tropics coincided with the period of
phytoplankton maximum (Fig. 5).

The phytoplankton is usually dominated by diatoms (Sournia, 1969;
Glynn, 1973). According to our observations, the important components
of the phytoplankton in the water above reefs Are the dynoflagellates of
the genus Porocentrum, as well as filamentous blue-green algae, washed
out from the periphyton and phytobenthos by the surf. If the blue-green
alga, Trichodesmium rubrum is developing in the surrounding waters of
the ocean, it appears in a significant quantity in the water above the
reef, as well, at times representing as much as 90% of the total
phytoplankton biomass.

In spite of the intensive water exchange, the distribution of
phytoplankton and its production above the reef are usually not
uniform: The maximum values are observed above the outer slope of the
reef (Br-FR zones), the minimum values in the lagoon. This may be
either a result of the consumption of the phytoplankton by the reef
fauna (Emery, 1968; Glynn, 1973) or a result of a more intensive
breeding of phytoplankton over the outer slope of the reef which is
enriched by the runoff of nutrients and biologically active substances
from the reef flat.

The primary component of the plankton in the water over the reef in
most cases is not phytoplankton, but rather bacterioplankton. The
biomass of phytoplankton over reefs usually does not exceed the limits
characteristic for oligotrophic waters the biomass of bacterioplankton
corresponds to the level of mesotrophic waters, and sometimes of
eutrophic waters of the ocean. The biomass of bacteria exceeds the
biomass of phytoplankton by an average of 5-10 times, production--by
1.5-2 times. The total population of bacteria in the water above the
reef averages 0.5-1.5*10^ cl/ml, their biomass--20-80 mg C/m-^ (0.2-0.8
g/m^ wet mass). In certain cases, the population of bacteria may reach
3 million cl/ml with a biomass of over 130 mg C/m'^. These magnitudes
were noted in New Guinea (organic-rich terrigenous runoff) and in the
lagoon of the polluted reef of Kaneohe Bay, Oahu, Hawaii (Sorokin,
1973e). ^bst of the bacterioplankton consisted of rod-shaped forms.
About 30% of the cells were joined into aggregates--accumulations 5-15
wn in diameter. Their formation is a result of the property of a part

180

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181

Fig. 5. Seasonal fluctuations in
population of diatoms (D, cl/«,) and
veliger gastropods (V, 10^ indiv.),
settling each month onto an area of
1 m^ (according to Glynn, 1973).

nr I I m m 7 m m m a x

of the bacterial population, that iL furms aggregations in the pro.. ess
of multiplying (Sorokin, 1971a, b, 1973c), rather than a result of the
cementing effect of the coral mucus, as was assumed earlier (N.B.
Marshall, 1968; Johannes, 1967).

The maximum values of biomass of bacterioplankton avq usually noted
in the shore zone, where the surf washes the microflora from the bottom
sediments, and also in the frontal zone of the reef (Br-FR zones). Here
also, we frequently see the greatest value of bacterial production. The
values of daily production of bacterioplankton varied within limits of
10-50 mg C/m^, the daily P/B ratio was 0.2-0.4 in the lagoon and 0.5-2
over the outer slope of the reef. The low values of P/B coefficient in
the lagoon, particularly along the shore, atq. apparently related to the
input of a large quantity of benthic microflora, slowing the
multiplication rate in the water column.

The information available on the zooplankton of the reef waters is
sparse and contradictory (Johannes et al., 1970; Emery, 1968; Glynn,
1973). It is difficult to observe, since most of it hides during the
day in the sand and in stands of macrophytes, and appears in the water
only at night. Also, the biomass of mesozooplankton on the reefs is
subject to great seasonal variation (Fig. 5), since a significant
portion of it consists of the meroplanktonic larvae of benthic animals
(M. J. Allen, 1957). Data on the biomass and seasonal changes in
organisms of the microzooplankton (nauplial stages of copepoda,
infusoria) are severely lacking.

The coral communities d^vQ inhabited by a rich and varied
ichthiofauna. A significant portion consists of benthophages, which
feed along with benthic animals also on detritus, algae, periphyton, and
also living corals. The biomass of fish in reefs was estimated as 100-
300 kg/ha (Glynn, 1973). The planktonophagous fish inhabiting the area
around reefs is dominated by juvenile oceanic pelagic species, which
find good feeding conditions here.

182

2.6 Nutrition and Food Connections of Reef Fauna

For many common species of the infauna, and particularly for the
corals, a diversity of modes of feeding is characteristic, including
symbiotic autotrophy. Among the animals which have plant symbionts in
addition to the corals are the actinia Anthopleura, the soft corals
Zooanthus, the colonial actinia Palythoa, the gastropod mollusks
(TridachTa, Placobranchus) , and the bivalve mollusks (Tridacna ,
Hippopus) . The Tridacna, which dre quite large (length up to 1 m,
weight up to 250 kg), frequently play a significant role in the
productivity and accumulation of calcareous material on the reefs.

The symbiotic algae include the dinoflagel lates (Zooxanthellae) ,
the green algae (Zoochl orel lae) and individual chloroplasts of free-
living siphon algae, consumed by their animal hosts (Tridachia) . These
chloroplasts accumulate and function in special mucous glands of the
mollusks (Trench, 1971).

In addition to the ability to use solar energy for autotophic
nutrition, most coelenterates (corals, hydroids, actinia) as well as the
bivalve mollusks, sponges and Ascidia, are able to effectively utilize
dissolved organic matter in sea water (Sorokin, 1973a; Sorokin,
Wyshkwarzew, 1972). The consumption of dissolved organic matter begins
at a concentration of some tens of pg/£ (Fig. 4), whereas the
concentration of low-molecular organic matter in the water above a
eutrophic coral community is 0.2-1 mg C/£, with the total content in the
water of 3-5 mg C/£. Its liberation by the benthic community in the
process of photosynthesis could be as high as 0.3-0.6 mg C/£ per day
(Khaylov, 1971). Consequently, we can assume that the dissolved organic
matter of sea water, like the plankton and seston, participates in the
transfer of energy between reef biotopes, bonding them into a unified
ecosystem.

Another important source of nutrition for benthic filter feeders on
the reef is the bacterioplankton. Studies by the radiocarbon method
have shown (Sorokin, 1973e; Sorokin, 1973b, c) that among the filter
feeders which feed intensively on the bacterioplankton are the sponges,
bivalve mollusks, ascidians, polychaetes (serpul 1 ides, sabellides),
corals, hydroids and zoantharians (Palythoa) . The most active consumers
of bacterioplankton were found to be the sponges, polychaetes and
bivalve mollusks, for which, at a concentration of bacterioplankton near
the natural level of around 1-2«10° cl/ml , the filtration rate reaches
600 £/g of organic carbon of the filterers' body per day. The
filtration apparatus of these animals is so highly perfected that they
can consume bacteria with a biomass of less than 10 mg/m-^--50-100 times
lower than the natural concentration of bacterioplankton in the water
over a reef and 3-5 times lower than that of the surface waters of the
neritic zone of the ocean. Consequently, they can utilize
bacterioplankton from the oceanic water passing over the reef and thus
include this external source of energy in the metabolism of the reef.

The daily ration of the active filter feeders of the reef, feeding
on bacterioplankton at its natural concentration, is 5-50% of their body
weight, sufficient to compensate for the expenditures for metabolism.
For the sediment feeders (madreporarians , zoantharians, hydroids) and

183

coarse filter feeders, which filter out primarily bacterial aggregates
measuring more than 5 m in diameter, bacterioplankon makes up only a
portion of their daily ration. For example, the coral Pocillopora . by
feeding on bacterioplankton and dissolved organic matter with a
concentration near the natural concentration, can compensate for about
1/4 of the metabolic expenditures. It must be considered that the value
of the bacterioplankton for the corals could be more in the nutrients
they contain than in the energy which they receive in sufficient
quantity from the symbiotic Zooxanthel 1 ae.

Phytoplanktcn, as a source of food for filter feeders, in most
cases plays a much less significant role than does bacterioplankton.
Its biomass in the water of coral biogeocenoses is usually 5-10 times
less than that necessary for the normal nutrition of the reef
organisms. Only in the productive zones of the ocean or during periods
of the maximum development of phytoplankton in oligotrophic waters can
we expect participation of phytoplankton in the nutrition of benthic
filter feeders and sediment feeders of the reef to be significant. The
question of the value of phytoplankton as a source of food for the coral
has not yet been answered. The available data indicate that the
madreporarians practically do not consume it and are not capable of
digesting the plant cells (Yonge, 1931; Sorokin, 1973a). However, the
alcionarians and zoantharians can feed on phytoplankton (Sorokin,
1973e).

We can also suppose the microzooplankton has to be a significant
component in the trophic connections of the reef. However, there dre no
quantitative data available on this question. The mesozooplankton of
the reef is consumed both by the corals themselves (Porter, 1974) and by
the hydroids, Zoantharia, Actinia, Gorgonaria, Calani and Polychaeta.

Attempts to estimate the food value of net zooplankton for the
coral have been made on the reefs off the Bermuda Islands (Johannes et
al., 1970). It was found that even with complete consumption of the
zooplankton carried above the reef by currents by the coral (Pi ploria) ,
it could compensate for only about 5% of the expenditure of the coral
community for metabolism. However, the biomass of zooplankton on the
reefs in eutrophic regions off Florida and the Laccadive Islands is
quite high--up to 0.2-0.5 q/m^ (Emery, 1968; Tranter, A. Jacob, 1969).
The meroplankton is also quite numerous, particularly at night.

The food resources created by benthic algoflora and the bacterial
population of the sediment and reef periphyton are used by many benthic
invertebrates and fish. Many of them take in the bottom sediment
nonsel ectively : coral sand, detritus, regeneration sediment, formed
among accumulations of dead colonies of coral (Bakus, 1973). As was
shown earlier, the bottom sediments of the reef contain an exceptionally
rich microflora and phytobenthos. It is therefore not surprising that
even nonselective consumption is energetically expedient for animals.
Experiments using C^^ have shown that the Holothurioidea Ophiodesma and
Gastropoda Nerita digest the microflora contained in the sediment and
can fully satisfy their nutient requirements with it alone (Sorokin,
1973e). The quantity of bottom soil consumed per day by these animals
frequently exceeds their own weight. In a year, the entire upper layer
of sand, several centimeters thick, passes through the intestines of the

184

Holothurioided. An individual about 30 cm long passes 100-200 g of sand
through its gut each day (Backus, 1973). In addition to the
Holothurioided and Gastropoda, the benthic sediment is also intensively
consumed by many species of fish. Some 25 t of calcareous material
passes through the intestines of fish feeding on the bottom sediments,
periphyton, and corals on the reef off Panama each year for each ha,
with a population density of these fish of 6 individuals for each 10 m^
(Glynn, 1973).

The periphyton is the main food of most of the reef Gastropoda, as
well as crabs, sea urchins and fish. The calcareous algae and corals
are eaten by the parrot fish, which use their strong jaws to scrape the
periphyton from the rocky base and dead corals (Randall, 1974).

The direct consumption of macrophytes by the reef fauna is
relatively slight. The algae are partially utilized by certain
gastropods, sea urchins, fish and Chelonia. Nevertheless, the
macrophytes play an important trophic role in the reef community as a
source of usable dissolved organic matter and detritus. The massive
species of macrophytes (Thalassia , Sargassum, Syringodium, Chnoospora,
Caul erp) cover significant areas. Photosynthesis in their stands on the
reef may be as great as 10-20 g C/m^ per day (Odum et al., 1959). The
quantity of products of photosynthesis liberated by the macrophytes into
the water amounts to 10-20% of the daily production (Khaylov, 1971).
Consequently, the production of dissolved organic matter over the
underwater meadows of macrophytes may be as great as 1-3 mg C/m^ per
day, which is sufficient for the feeding of many species of benthic and
planktonic filter feeders, including corals. As a result of the death
of the algoflora, a mass of detritus is formed (Goreau, Goreau, 1973);
for example, on one island of the Great Barrier Reef, about 1 kg/m'^ per
yedr. The main nutrient component of the detritus consists of the
microflora and protozoa which inhabit it abundantly (Fenchel, 1970).
The detritus serves as a source of nutrition for a rich detritophage
fauna. Some of them collect the detritus from the bottom (gastropods,
Holothurioidea, sea urchins, various Crustacea, Polychaeta, many fish)
while others filter out the detritus stirred up by the surf from the
water.

2.7 Conclusions

The materials analyzed above, concerning the structure of modern
coral reefs, like the data from fossil reefs (Ladd, 1969; Copper, 1974) ,
show that the coral community forms a clear biogeocenosis, consisting of
a system of specialized biotopes and their populations. This system is
similar, even under greatly differing conditions, e.g., on barrier
reefs, near large islands and continents, in highly productive waters
with rich terrigenous runoff and in atolls in the oligotrophic waters of
the trade currents. The reason for the similarity of the structure and
level of productivity of the reefs in these various regions is that
conditions in the coral communities, in contrast to communities of the
pelagic zone, are controlled primarily not by external physiochemical ,
but rather by internal biological factors. The coral community
constructs a specific limestone structure--the reef. It might be
thought of as a kind of a cultivator, in which a definite spatial

185

distribution of biocenoses is created, with a definite orientation
regarding the flow of solar energy, protection from destruction by wave
action, tectonic downwarping, etc. Given the relative constancy of the
temperature in the tropics, the conditions of life in the reef community
Are regulated primarily by the influence of the intensive vital activity
of its organisms. This is particularly true of the processes related to
the cycle of nutrients, which Are practically completely controlled in
the reef by the community itself. The regulating influence of the
community on environmental conditions makes them largely predictable,
which, in turn, allows specialization of a significant portion of the
flora and fauna (Grassle, 1973; Golikov et al . , 1972).

These same properties of coral biogeocenoses apparently explain
their unusually high productivity largely counteracting the limiting
effect of the shortage of nutrients which limits the productivity of the
aquatic ecosystems of the tropical zone. The primary portion of
photosynthetic production of the reef is created under conditions of a
semiclosed cycle of nutrients. These conditions exist in the host
organisms of symbionts and in communities of periphyton organisms, where
the producers and reducers are joined into a single structure. We must
assume that this semiclosed cycle of biogens is characteristic to some
extent for colonies of calcareous algae as well. These colonies have a
porous surface, overgrown with microflora (DiSalvo, 1973), which can
mineralize the organic phosphates liberated by the algae.

Another factor in the high productivity of the coral biogeocenosis
is, apparently, the existence of extremely effective mechanisms for
extraction and utilization of organic forms of nutrients from the ocean
water passing over the reef. The mean content of organic forms of
nutrients in the surface waters of the tropical zone of the ocean is
0.2-0.4 pg-atom/Jl of phosphorus and about 1 p-atom/Ji of nitrogen, as
great as the content in the water of the temperate zones (Sapozhnikov ,
1971). Most of this matter is found in the composition of relatively
stable dissolved organic matter which is utilized by the periphyton
microflora of the reef in large quantities. Possibly, it is the
presence of this external source of organic matter and nutrients which
represents one of the main factors in the unusually rich development of
periphyton on all solid surfaces and in the large-grained sediment of
the reef.

The richness of the microflora of the bottom sediments depends
directly on the degree of development of living corals in the biotope,
whereas the development of the periphyton, microflora and algoflora do
not depend on this factor (Sorokin, 1975b). The periphyton grows even
in places where the corals have been completely smashed by a typhoon.
The periphyton community of the reef, particularly in the frontal zone
and on the surface of the reef flat, exists by utilization of nutrients
and, to some extent, of the organic matter from the ocean waters passing
over the reef.

Another portion of the organically bonded nutrients in the ocean
water passing over the reef is present in the form of suspended organic
matter, pseudoplankton, and plankton. The reef community actually is a
powerful biological filter, capable of utilizing this source almost

186

completely. The corals trap zooplankton and protozoa, the filter
feeders and sediment feeders trap the phytoplankton and microflora. The
high effectiveness of the reef as a biologic filter and the significant
volume of neritic water which passes over the reef, with a high
concentration of plankton, allow the coral community to receive such a
great influx of organically bonded nutrients that it compensates for the
unavoidable losses of nutrients liberated in the process of metabolism
and carried away by the ocean water passing over the reef. The positive
balance of nutrients in the processes of exchange between the reef and
the water passing over it is apparently the key to the solution of one
of the most baffling peculiarities of the reef metabolism: the clear
accumulation of organic matter in the community, in spite of its visible
and tremendous output into the waters of the ocean. It is clearly
visible to the naked eye that the water approaching the reef is
transparent, with little organic sediment, while the water flowing away
from the reef is turbid, rich in suspended matter and organic aggregates
(N. B. ^c^rshall, 1968; Johannes, 1967). How is the essentially positive
balance maintained, in terms of organic matter, with these losses and
with the intensive destruction of organic matter within the community?
Apparently, the reef community is so organized that, being under optimal
conditions of illumination and temperature and having an unusually high
content of chlorophyll per unit area, it creates a sufficient quantity
of organic matter to compensate for losses due to erosion and
destruction. We must consider that the organic matter which is lost and
destroyed is poorer in nutrients than that consumed by the community
from the water passing over the reef. Without this mechanism, providing
a more positive balance of nutrients in exchange with the surrounding
water, the formation of the coral biogeocenoses would hardly be
possible.

It is characteristic of coral communities to have extensive porous
surfaces, overgrown with an active and rich periphytonic microflora.
Its functioning occurs under optimal conditions of temperature and
oxygen supply. Under these conditions, similar to the conditions of the
air tanks of purification structures, the processes of bacterial
destruction are intensified, like chemical reactions on a surface of
porous platinum. It can be assumed that the microbial population of the
periphyton can assimilate those fractions of the organic matter which
make up the predominant portion of the total dissolved organic matter of
sea water, but are difficult for bacterioplankton to oxidize in the
pelagic zone. Therefore, although the waters of the ocean passing over
the reef show an increased content in labile organic matter (Sorokin,
1973b), it is probable that their content of a stable organic matter and
particularly, the nutrients bonded with it, must decrease as the ocean
water passes a reef.

This system of exchange of coral communities with the water passing
over the reef requires further testing, but we can assume that, given
the tremendous area of coral reefs, the intense destructive activity of
the periphyton microflora is of global significance in processes of
biogeochemical cycling of organic matter in the world ocean. The coral
reef communities should be looked upon as the location of oxidation of a
significant portion of the stable organic matter (water humus) in sea
water. It should be expected that the constancy of concentration of

187

organic matter in the waters of the ocean--dbout 2 mg C/£--is controlled
to some extent by the periodic passage of the entire volume of water in
the world ocean over coral reefs as global circulation occurs.
According to our calculations, the time required for this process is not
so great in the geologic scale of time: about 40,000 years.

Investigators studying coral biogeocenoses report a high degree of
maturity of the coral reef ecosystems (Grassle, 1973). The signs of
maturity include the predominance of long-living forms with slow growth
rates, as well as the high predictability of conditions of the growth
medium and a high degree of specialization of many mass species which we
mentioned earlier (Golikov et al., 1972). The maturity of the reef
community is also revealed as we analyze the inherent complex
interactions between organisms as, for example, the hierarchy of
antagonistic interactions between corals (Lang, 1973), as well as the
developed ecologic metabolism.

The maturity of the reef biogeocenosis is also manifested in the
close energy interaction of the component communities. This interaction
basically follows two paths. The first path is the transfer of
dissolved organic matter liberated by autotrophs, detritus, periphyton
and benthic bacteria and algae, washed by the surf from the epibiotic
associations and bottom sediments. The tide currents over the reef are
mostly of an advancing and retreating nature. As the tide rises,
practically the same water which left the reef when the tide fell
returns to it. At low tide, the water leaving the reef passes over its
frontal slope, where an intensive multiplication of microplankton
occurs, and is held there. Therefore, the corals and other benthic
filter feeders and sediment feeders, living on the outer slope of the
reef, can utilize the energy reserves of the organic suspended matter
washed from the shallow zone of the reef. Another path in the trophic
connection of the biotope of the outer slope with the shallow zone is
the "runoff" of detritus, bottom sediments and clastic material in the
direction of the fore-reef. At the same time, the corals and macroalgae
growing abundantly on the outer slope enrich the water with dissolved
organic matter, which is carried by the tidal flow into the shallow
portion of the reef and there consumed by the periphyton microflora. We
must, therefore, consider the point of view (Yonge, 1963; Ladd, 1969)
that the biotopes of the outer slope of the reef Are not connected in
any way with the biotopes of the shallow portion of the reef (reef flat
and lagoon) to be incorrect.

The complex and intensively functioning ecosystem of the coral reef
is \iery sensitive to anthropogenic effects: pollution, eutrophication ,
overfishing. Pollution and eutophication result in a shift of the cycle
of organic matter in the direction of predominance of destructive
processes, decrease of the oxygen content, development of the process of
reduction of sulfates to hydrogen sulfide, appearance of reducing
sediment. All of this may cause massive death of corals and of the
fauna which populate it, rapid development of macrophytes, Zoantharia
and Actinia, which inhibit the growth of corals and replace them
(DiSalvo, 1973i Banner, 1974; Sorokin, 1971b, Sorokin, 1973b). It is
thought that the harvesting for their beautiful shells of large numbers
of some gastropod mollusks such as Hazonia tritonis, which are the

188

natural enemies of the sea star Acanthaster planci, has been one cause
of the sudden increase in the number of these animals, which have
consumed over hundreds of square kilometers of corals (Endean, 1973).
Extensive harvesting of tridacna and trepangs reduces the biof il tration
activity of the community and decreases the intensity of processing of
bottom sediments. It is therefore necessary to turn the most serious
attention to the protection of coral communities as one of the most
important biologic systems of the ocean, and of the biosphere as a
whole.

189

3. Fouling Communities.
(Ye. P. Turpaeva)

The term "fouling" is usually used to mean a complex of animals and
plants, which settles onto artificial structures. The formation of
fouling communities on structures submerged in the water depends on the
capability of certain species of animals and plants to develop
successfully in a situation created by man. The basic components of
fouling communities include the attached forms: cirripedian
crustaceans, bivalve mollusks, hydroids, Bryozoa, sedentary polychete
worms, sponges, Tunicata, as well as certain algae. Furthermore, the
overgrowth includes mobile animals: crabs, Nudibranchiata, errant
Polychaeta, Nematoda, Harpaticoida, Pycnogonida. The total number of
species of animals and plants recorded in the fouling communities
reaches 2,000.

The qualitative composition of the fouling communities on all
artificial substrates is determined by the composition of the flora and
fauna of the surrounding regions, the number of species fouling being
always less than the number of species inhabiting the region. The
epibiotic fauna of the littoral regions usually number 50-100 species.
The total number of species in macroscopic fouling communities in the
open seas of the USSR is not over 25, in the southern seas--10. Fully
formed fouling biocenoses in the southern seas of the USSR usually
consist of 3-5 species (2-3 attached, 1-2 unattached), while the
quantitative development of one of the attached species is usually
significantly more than the development of the remaining forms. A
similar peculiarity is characteristic of the oligomyctic benthic
biocenoses. Epibiotic biocenoses represent an extreme case in this
respect.

The species which settle in epibiotic associations usually reach
significantly greater quantitative development than in natural biotopes;
correspondingly, the total biomass of fouling biocenoses is usually
great, frequently one or two orders of magnitude more than the biomass
of natural communities. For example, the biomass of the fouling
associations in the Sevastopol' Bay may reach 100 kg/m^, the fouling
associations of Balanus in Kerchenskiy Strait--40 kg/m^, the fouling
associations of hydroids in Taganrog Bay--15 kg/m^ (Turpaeva, 1971).

The overwhelming majority of species of animals which compose these
communities have a pelagic larval stage. The larvae of some mass
species from these communities (numerous forms of bivalve mollusks, and
cirripedian crustaceans, live in the plankton for rather long periods of
time--up to several weeks). In temperate water, the breeding of fouling
organisms stops in winter. They winter over in the mature stage, and
begin to breed again in the spring, with the beginning of the
development of phytoplankton. In accordance with this, the settlement
of organisms and development of the epibiotic biocenoses are also

190

seasonal processes. The larvae of the various species of animals settle
at different temperatures, which defines the sequence of appearance of
the various species in the composition of the fouling assemblages and
determines the succession of these biocenoses (Zevina, 1972).

Thus, for the fouling communities, which develop in the internal
seas and littoral oceanic regions, a small number of species
(oligomyctic nature), a high biomass and the seasonal changes in the
process of formation are peculiar.

Studies of fouling processes in the oceanic waters are only
beginning. The formation of large masses of fouling in the open ocean
is limited by the lack of a stable substrate. Although organisms which
are not inhabitants of the littoral regions are always found on the
hulls of ships which follow the transoceanic routes, the oceanic forms
alone never develop on ship hulls. We can make judgments concerning the
composition of fouling associations in various regions of the open ocean
at the present time by studying driftwood. Materials collected from the
northwest Pacific (Turpaeva et al . , 1976) show that oceanic fouling
communities are also characteristically oligomyctic, with a high biomass
and seasonal alteration of composition, related not only to seasonal
changes in the presence of pelagic larvae in the plankton, but also to
changes in the overall flow of the currents.

In spite of the seasonal changes in the composition of fouling
communities, their structure is always characterized by clear-cut
domination by a small number of species. The species which are dominant
in these communities are usually representatives of groups which are far
removed from each other in the systematic and ecologic aspect (Turpaeva,
1967). In these communities, there is no competition among dominant
species for food, and the negative effect which they have on each other
is minimized.

An example of such a structure is the fouling community on the
hydrotechnical installations of a metallurgical plant located at Zhdanov
on the north coast of the Azov Sea. Six mass species have been found in
this community: the hydroid Perigonimus megas, feeding primarily on the
copepod Calanipeda aquaedulcis; the cirripedian Balanus improvisus,
feeding on phytoplankton and small zooplankton; hydroid epibionts: the
infusorian Zoothamnium sp. and the bryozoan Boyerbankia imbricata,
feeding, apparently, on microplankton and small detritus; the predatory
nudibranchiate mollusk Tenellia adspersa and the euryphagous crab
Rhitropanopeus harrisii.

Many years of study of the composition of this community and the
ecologic-physiologic indices of its main species, both in nature and in
the laboratory, have revealed various types of interactions among them.

A complete system of symphysiologic (B. N. Beklemishev, 1951)
interconnections of this overgrowth community numbers some 40 direct and
indirect topical and trophic links, most of which function during the
spring and summer, when the larvae settle, the macroscopic epibiotic
organisms grow, and the community as a whole is formed. The various
connections of this system are not equal in terms of their time of

191

action, nature of effect on the population of dependent species or
intensity. The diagram (Fig. 6) shows the 16 most important connections
within this system.

The dominant species of the biocenosis is the hydroid. The second
species, in terms of abundance, is the Balanus. They usually settle in
May and develop simultaneously. Under favorable conditions, with a
favorable quantity of plankton food, the hydroid forms a thick cover on
the substrate within a month. Its branching stolons cover the Balanus
and hinder their access to the water and food--paired, indirect, topical
and tophic connection 1 develops, reducing the growth rate and, later,
the population of Balanus. Soon, Vorticella develop on the stolons of
the hydroid (direct topical connection 2) and the suppression of the
Balanus is increased (connection 3). The population of the Vorticella
on the stolons of the hydroids is regulated during this period by its
intraspecific indirect topical connection (4). In June, the Tenellia
appear in the community. They live on the stolons of the hydroids and
feed on the hydroids and Vorticella (direct topical and trophic
connection 5 and direct trophic connection 6). With a low population of
Tenellia, its food demands are met almost entirely by eating the
Vorticel^la, thus protecting the hydroids from being eaten by the
Tenel 1 ia~ri ndi rect trophic connection 8). If the population of Tenellia
is high, it not only eats out the Vorticella, but also suppresses the
development of hydrants to the extent that some portions of the colony
having none of them die and separate from the substrate. This improves
the conditions of nutrition of the Balanus, creating an indirect trophic
connection between the Tenellia and Balanus (7). The suppression of the
hydroids decreases the area of the substrate and the quantity of food
for new generations of Tenellia. The Tenellia population is regulated
by paired indirect connection 9, as a result of which, some of its
individuals are expelled from the hydroid colony and carried away from
the community by the flow of the water. In late June, the bryozoan
Boverbankia appears in the community, overgrowing the stolons of the
hydroids (direct topical connection 10), partially expelling the
Vorticella (indirect topical connection 11). In July, crab larvae begin
to settle. The young crabs grow rapidly, and are quite voracious. They
eat the Vorticella and Bryozoa (connections 13 and 14), and the
Calanipeda which they find among the hydroids, mysids hiding among the
stolons of the hydroids, their own juveniles (connection 16) and quite
eagerly eat the Tenellia and its clutches of eggs (connection 15).
After the crab appears, the population of Tenellia decreases rapidly,
and, therefore, the damage done by the Tenellia to the hydroids also
decreases. Since the predator has disappeared, the hydroid once again
begins to grow and, during the autumn development of zooplankton, the
colonies grow and multiply.

In order to even approach a quantitative evaluation of some of the
connections in this system, we utilized the method of mathematical
planning of experiments, which allowed us to vary the number of species
of animals interacting in the experiment. The experiment was undertaken
with four species--the hydroid, Balanus, Vorticella and Tenellia. We
studied the strength of the connections relating to two complexes:
suppression of the Balanus by hydroids (complex I) and the interaction
of the hydroid with the Tenellia (complex II). The experiments were

192

Micropl.iukton

Ph;.^oplankton

L>rvczo£

•'orti cellrl

Fig. 6. Diagram of symphysiologic
community in the Azov Sea. Connect
topical; c, Direct trophic; d, Indi
species, the abundance of which is
given connection. A double-ended a
populations of both species changes
the nature of the influence of the
species: + indicates an increase,
populations of both species changes
the nature of the influence of the
species: + indicates an increase,
show the connection numbers.

connections of an overgrowth
ions: a. Direct topical; b, Indirect
rect trophic. Arrows point to
changed under the influence of the
rrow indicates that the abundance of
. The signs by the arrows indicate
connection on the population of the

- indicates that the abundance of

. The signs by the arrows indicate
connection on the population of the

- indicates a decrease. The numerals

193

organized according to the plan of a full factor experiment (FFE-2^),
the experimental object was the Balanus, the factors were the
Vorticella, tenellia and hydroid. In accordance with the planning
matrix, each factor was represented at two levels: the upper (+) and
lower (-) levels. For the Tenellia and hydroid, the lower level
represents absence of the species in the corresponding versions of the
FFE, while the upper level represents its presence. The Vorticella, in
versions with a lower level, was periodically eliminated. The plan and
results of the experiment are presented in Fig. 7. As we can see from
the graph, significant suppression of the Balanus is observed only in
those versions in which the hydroid developed; tHe hydroid and
Vorticella developed well only when the Tenellia were absent, while a
high population of Tenellia was formed where the hydroid was present and
the Vorticella was periodically eliminated.

The results of the experiment allowed us to calculate the relative
intensity (ratio of value of partial effects to results of experiment in
those versions in which effect of given connections has been revealed)
of the connections which we modeled (Table 9). It was found that the
coefficients of relative effectiveness C for the various connections are
not the same, and change from comparatively small positive to high
negative values. For bilateral connections, the two coefficients of
relative intensity differed not only in magnitude, but also (in two
cases) in sign. The higher the value of negative coefficient C, the
greater the suppression of the dependent species; the higher the value
of the positive coefficient, the more favorable the conditions for
development of the dependent species; the lower the modulus of
coefficient C, the weaker the effect of the connection.

The values of coefficients of relative intensity produced for the
connections modeled were compared with the characteristics of
development of the animals or the status of the populations. To do
this, using the results of the FFE, we calculated the specific rate of
weight increase (C^) of the Balanus and hydroids. We found that the
specific rate of growth of the Balanus changed as a function of the
specific growth rate of the hydroid (Fig. 8). The suppression of the
Balanus was weakest when the three-member connection 7a was functioning
(Fig. 7 , version 8) with C^ of the hydroid less than 0.3. An increase
in the specific growth rate of the hydroid to about 0.4 was accompanied
by a severe inhibition of the growth of the Balanus. Comparison of the
coefficients c of the connections of complex I with the values of C„ for
the hydroid showed that the growth rate of the Balanus, with low growth
rate of the hydroid (less than 0.3), was determined by the conditions
under which the animals were maintained. With a further increase in C^
of the hydroid, the effect of symphysiologic connections appeared, the
intensity of which increased with an increase in the growth rate of the
hydroid. In turn, the specific growth rate of the hydroid changed as a
function of the Tenellia population (connection of complex II). Eating
the hydroid, the Tenellia constantly damages the hydranths, penetrating
their cover and sucking out the plasma. The damaged hydranths
regenerate after 3 or 4 days, but until this happens, the total food
intake of the hydroid colony decreases, and its growth is slowed. The
frequency of damage, obviously, is related to the population density of
the Tenellia, which can be estimated by the weight of the hydroid colony

194

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195

No.

Factors

O r—

- +

- + -

- + +
+ - -
+ - +
+ + -
+ + +

Hydroid,
mg/44 cm2

Tenellia Vorticella,
indiv. indiv./cm^

2M '/OH em $ffo mo .'20

Sff Wff

/Off 200 JOO VOOs

S /a !S 20 ff

Balanus ,
base diam. ,
mm

Fig. 7.
Balanus

Change in abundance of hydroid, Tenellia, Vorticella and

in various versions of a full factor experiment FFE-2-^. Number

of individual infusoria (a) and colonies (b) counted for Vorticella.

Fig. 8. Relation of specific growth
rate of Balanus to specific growth
rate of hydroid.

a/ o.z

C^f Hydroid

0.^

per individual mollusk. The variations of this quantity were found to
be slight: In version 7, each mollusk corresponded to about 6.5 mg of
hydroid, in version 8--about 3 mg. However, the specific growth rate of
the hydroid in version 7 was only 15% less than the control, while in
version 8 it was almost 70% slower, and the relative intensity of
connections 8 and 5 differed by a factor of 16 (-0.61 and -10.02).

196

The influence of symphysiologic connections of both of the
complexes studied was thus manifested in a very narrow range of change
of the effective factor--the specific hydroid growth rate (complex I)
and the relative Tenellia population density (complex II)--within limits
confined to the "effective range" of the complex of connections.
Outside the limits of this range, with a lower intensity of the
effective factor the influence of the connections is not felt, and the
development of the dependent species is determined by its ecologic
peculiarities under the specific conditions at hand; with higher
intensity of the effective factor, the dependent species is destroyed.
In turn, changes in the intensity of the effective factors are
determined by the presence of modifier species: the Vorticella and
Tenellia. The intraspecific connection coefficients of both these
species were found to be much higher than the interspecific connection
coefficients. This agrees with the ecologic theory, according to which
intraspecific competition, with high populations, is more acute than
interspecific competition (Shorygin, 1939, 1946).

Long-term changes in the intensity of connections can be presumed
in those cases when a slow increase in biomass or abundance of the
conditioning species occurs. However, a high abundance or biomass of a
conditioning species cannot be used as an indication of great intensity
of a connection. According to the materials of the FFE, the greatest
value of relative intensity was that of connection 5 (version 8), where
the population of the conditioning species (Tenellia) was quite low
throughout the entire experiment, while the development of the dependent
species (hydroid) was suppressed at the very beginning. The
symphysiologic connections with high intensity of action modeled in the
FFE rapidly stopped the growth of the population of the dependent
species by its elimination; connections with low intensity acted slowly,
and the dependent species continued to develop.

In the natural overgrowth community, the symphysiologic connections
modeled in the FFE function at different times. The time divergence of
the action of the various connections is caused, on the one hand, by the
seasonal differences in the time of settling of larvae, determining the
seasonal succession of complexes of the connection, and, on the other
hand, by time differences in occurrence of the maximal abundance of the
various species of animals, defining the sequence of functioning of the
connections of each complex. For example, in spring, after settling of
the hydroid and Balanus larvae, when the young stolons of the hydroid
are free of epibionts, the action of connection 1 is evident. After
some time has passed, the Vorticella develops on the 4 to 6-day old
stolons of the hydroid, and connection 3 begins to function, which, with
intensive development of the hydroid, usually causes mass mortality of
the young Balanus. In mid- summer, with mass development of the
Tenellia, connections begin to function which suppress the hydroid; at
first connection 8, decreasing the growth rate of the colonies, then
connection 5, suppressing its vital activity. As the Tenellia
population increases, intraspecific connection 9 begins to function, the
intensity of which apparently gradually increases. After the vital
activity of the hydroid is suppressed, the intensity of connection 9
reaches its maximum, most of the individual Tenellia are expelled from
the community, and the remaining small portion, temporarily go over

197

entirely to feeding on Vorticella, until the hydranths regenerate
(connection 6). Thus, in the overgrowth community investigated, a
sequential change is observed in the effect of weak and strong
symphysiologic connections. During functioning of the weak connections,
the abundance and biomass of the dependent species increase. During
functioning of weak positive connections, the increase of abundance and
biomass is determined by the ecologic peculiarities of the species
(fertility, growth rate, rate of settlement of larvae). The effect of
weak negative connections is superimposed on the effects of these
peculiarities, and the development of the abundance and biomass of the
dependent species is retarded. Strong negative connections cause a
sharp decrease in the abundance of the dependent species.

It can be assumed that the sequence of functioning of connections
and alternation of weak connections, acting slowly, and strong
connections of brief duration, combine to determine the oligomyctic
nature of the overgrowth community and sharp changes of their dominant
species with time.

198

4. Benthic Shelf Communities (A. A. Neyman)

In this section, we shall discuss benthic shelf biocenoses beyond
the limits of the plant zone, i.e., at depths of over 10 m.

The food resources of the inhabitants of this zone consist of the
detritus which reaches the bottom layers of water and the floor from the
photic layer. This greatly simplifies the composition of the benthic
shelf biocenoses, since producers and phytophages are absent, while the
detritus consumers remain (see 1 1 1. 5), along with the low-mobility
predaceous forms.

Quantitative investigations of the benthos in large water areas are
performed using bottom samplers, which trap only the non-moving and
slowly moving animals. Therefore, bottom-sampler collections can be
used only to study the competitive relationships between animals of a
single trophic level. Predator-prey relationships are played out
between representatives of the low-mobility benthos and necton
(benthophagous fishes) and migrating benthos (e.g., crabs), i.e., they
go beyond the framework of the biocenoses which can be studied by means
of bottom samplers (L. G. Vinogradov, 1963; Vinogradov, Neyman, 1965).

V. P. Vorob'yev (1949) suggested a method of differentiating
biocenoses according to species dominant in terms of biomass. This
method has been widely used in Soviet marine research. The method of V.
P. Vorob'yev is quite simple and, at first glance, quite formal: in a
bottom-sampler sample, the species which dominates in terms of biomass
is determined; stations at which the same dominant species is found are
combined into a biocenosis. If these stations are placed on a map, as a
rule, we find that stations relating to a single biocenosis are quite
regularly placed (A. P. Kuznetsov, 1963, 1970; Neyman, 1963a, 1971).
Station-by-station comparison of the benthos with data on the particle-
size distribution of the bottom deposits reveals (Neyman, 1963b) that
each biocenosis is characterized by its own type of particle-size
distribution, and the particle-size distribution differences of similar
biocenoses (within a single trophic zone) are quite clear, though not
great: The same size fraction of bottom soil predominates, but the
degree of dominance and fraction of the corresponding particles differ
(Fig. 9). Thus, a biocenosis distinguished by the method of V. P.
Vorob'yev is a natural formation, owing its development to fine
differences in the process of sedimentation within the limits of a
single trophic zone.

N. P. Bubnova (1971, 1972) studied the process of nutrition of two
detritophagous bivalve mollusks in the White Sea— Macoma baltica and
Portlandia arctica--inhabiting soils with different contents of clay
particles. She demonstrated that the association with different soil
types of these mollusks was directly related to differences in their
capability to sort the bottom deposits: Portlandia cannot live on

199

'U

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A

.V

f

/

J

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B

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! Z S U 5 D 7 B / 1 J ^ J S 7 S
Particle diameters (dir.iensional classes)

Fig. 9. Relationship of particles of various diameters in soils in

bottom sections occupied by different biocenoses. Particle diameter,

mm: 1, >2; 2, 2-1; 3, 1-0.5; 4, 0.5-0.25; 5, 0.25-0.1; 6, 0.1-0.05;

7, 0.05-0.01; 8, <0.01. Biocenosis A: 1, Macoma calcarea;

2, Yoldia hyperborea; 3, Megayoldia thraciaeformis.

B, Nuculana pernulaT 1, in Bering Sea; 2, in Gizhiginskiy Bay of the

Sea of Ohotsk; C: 1, Ophiura sarsi ; 2, £. leptoctenia. D:

1 , Brisaster latifrons; 2, Chindota ochotensis; 3, STernaspis scuta ta;
4 , Axiothella catenata. E : 1 , Venericardia crebricostata;

2, Sernpes groenlandicus; 3, Clmocardium ciliatum.

200

coarse-grained soil, due to its weakly developed apparatus for soil
sorting, meaning that it cannot receive a sufficient quantity of food
there. L. V. Sanina (1975), using the example of sestonophagous
mollusks of the northern Caspian, showed that their distribution also
depends on the ability to sort organic particles from a suspension with
varying contents of mineral particles.

The use of the method of V. P. Vorob'yev, in combination with the
study of the ecologic habit and methods of feeding of the main species
making up biocenoses, has led to the conclusion that the core of a
biocenosis consists of minimally competitive species, (Birshteyn, 1947;
Vorob'yev, 1949; Ivlev, 1955; A. P. Kuznetsov, 1960; Sokolova, 1960;
Turpayeva, 1948, 1949; Shorygin, 1955), because of the membership of the
primary species of the biocenosis in different trophic groupings. The
simultaneous existence of representatives of various trophic groupings
is possible because they feed from different zones (levels) of the
bottom sediments. Depending on which of the feeding zones contains the
greatest quantity of nutrient substances in a given biotope, one or the
other trophic grouping will be dominant in the biocenosis. The greatest
competition occurs between representatives of the same trophic grouping.

However, there are biocenoses, the core of which consists of
species of a single trophic grouping. Ye. P. Turpayeva (1948, 1949) has
suggested that there may be fine differences in the nature of feeding of
species of a single trophic grouping, although she had comparatively
little data to work with. A. P. Kuznetsov (1960, 1963) is of the same
opinion. At the present time, a great deal of material has been
accumulated concerning the composition of shelf biocenoses of the seas
of the USSR and other regions of the world ocean, and these statements
can be made specific. For example, on the shelf of the eastern portion
of the Bering Sea, there is an extensive zone of sedimentation at a
depth of 50-150 m. The conditions are right there for rapid development
of detritophages, particularly gatherers. Extensive areas of the bottom
are occupied by biocenoses of Macoma calcarea, Yoldia hyperborea,
Nuculana pernula and hlucula temus, and in each of the biocenoses, all
of these four species are included in the core of the biocenosis. They
are all gathering detritophages. This composition of detritophage
biocenosis is, obviously, a result of the abundance of food at their
feeding level--detritus on the surface of the bottom deposits. K. N.
Nesis (1965) believes that an abundance of food at a given feeding level
leads to the appearance of biocenoses with a trophically homogeneous
core. This is proved, perhaps, by the fact that these same biocenoses
on a narrow shelf with relatively little sedimentation, have a different
core composition, containing sestonophages and nonselective
detritophages, as can be seen in the example of the biocenosis of
Macoma calcarea in the eastern Bering Sea and eastern Kamchatka.

201

Eastern Part of Bering Sea
Position as to Biomass Type of Feeding

1.

Macoma calcarea

leathering

2.

Yoldia hyperborea

II

3.

Nuculana pernula

4.

Nucula tenius

II

Eastern Coast of Kamche

itka

1.

Macoma calcarea

Gathering

2.

CI inocardium ciliatum

Sestonophage

3.

Nicomache limbricalis

Swal lowing

4.

Ampelisca macrocephala

Sestonophage

Analysis of the composition of biologically homogeneous biocenosis
cores shows that their composition practically never includes more than
one species of the same genus--a rule noted by Elton (1946). Similar
species apparently have similar types of feeding, this similarity being
expressed not only in that they feed from a single source of food, but
also in that their method of capture of food and other peculiarities are
similar. In other words, similar species belong to a single life form
and occupy a single ecologic niche. Similarity of the nature of feeding
of closely related species is confirmed by the analysis of association
of two pairs of similar species (Yoldia hyperborea and
Megayoldia thraciaeformis; OphiurlTleptoctenia and 0. sarsi ) in the
eastern Bering Sea with types of bottom: The biocenoses of species of
each pair are found in this area on practically identical bottoms (Fig.
9). Competition in this case is avoided due to the spatial separation
of closely related species, which have different zoogeographic
association and inhabit zones where different water masses are in
contact with the bottom (Neyman, 1963a). The theory of parallel
communities is based on the spatial divergence of similar species
(Thorson, 1957) in which representatives of one life form, but with
different requirements for temperature or salinity, dominate.

Thus, even an abundance of food, leading to the development of a
core of a biocenosis of species of the same trophic grouping does not
eliminate the need for the species to differ as to type of feeding. For
sestonophages, the possibilities for food differentiation are great, if
only because they can be rather finely divided as to levels. The
swallowing detritophages can also be divided in the same way--they can
feed from the bottom, burrowing into it to various depths. Gathering
detritophages do not have this capability--they can feed only from the
surfaces of the bottom. Therefore, difference in the nature of feeding
of gathering detritophages included in the core of a biocenosis must be
quite precise. This leads to yet another rule: The core of biocenoses
consisting only of gathering detritophages includes representatives of
only one zoogeographic or, in the language of G. V. Nikol'skiy (1947),
faunistic complex, probably because in order to achieve the precise
differentiations in feeding, long-term joint existence in the zone of
contact with the bottom of a single water mass is required.

202

The regularities outlined above concerning the composition and
distribution of benthic biocenoses were obtained upon detailed study of
benthic biocenoses on the shelves of arctic and boreal waters.
Analogous data concerning the shelves of Antarctic waters are sparse.
However, on the shelf and in the fjords of the south Orkney Islands,
basically the same composition of biocenoses and the same variation of
their distribution with the nature of the benthos of the tropical
shelves differs from that of the subpolar shelves in that there are
significant sections where the trophic zonal ity is disrupted or where
the detritophages, particularly swallowing detritophages, disappear from
the composition of the benthos. The same differences have also been
noted in the composition of biocenoses. Whereas in the shelf biocenoses
of the subpolar waters, all trophic grouping of nonpredaceous benthic
invertebrates are practically always represented, in the shelf
biocenoses of the subtropical and tropical waters, usually only one or
two trophic groupings are present.

203

5. The Trophic Structure of the Benthic Population
of the Shelves. (A. P. Kuznetsov, A. A. Neyman)

In recent decades in Soviet oceanography, studies of the trophic
characteristics of the benthic population have been greatly developed.
Domestic expeditions have accumulated significant materials (over 3000
samples) of the bottom population of the shelves of the world ocean,
collected by a single methodology--by means of the "Okean" bottom
digger. This allows us to make a judgment concerning the peculiarities
of the composition and distribution of the benthos at depths from 10-20
m down to the upper levels of the slope (300-500 m) (Neyman, 1971). The
studies have encompassed all geomorphologic types of shelves in various
geographic zones.

The detailed studies of Ye. P. Turpayeva (1953, 1954) allowed her
to work out a classification of marine benthic invertebrates on the
basis of the source and method of capture of food. Studying the bottom
population of the Barents Sea, Ye. P. Turpayeva distinguished the
following trophic groupings: "swallowing"--inhabiting the surface
layers of bottom deposits and swallowing the bottom whole; "gathering"--
gathering detritus from the surface of the bottom; "A filterers"--
feeding on matter suspended in the thin layer of water along the bottom;
"B filterers" (active filter feeders)--feeding on layers of water
located higher above the floor; "waiters"--receiving their food from the
same layer as B filterers, but passively.

The nonpredaceous benthic invertebrates feed on the organic matter
suspended in the water or in bottom deposits; therefore, the quantity of
food available to them in any given section of the bottom is directly
dependent on the productivity of the overlying photic layer. The
abundance of food for predaceous animals (benthophagous fish, large
crustaceans, etc.) depends on the distribution of nonpredatory
invertebrates. Therefore, in studying the connection of the
distribution of benthos with oceanographic characteristics (biotic and
abiotic), we must first turn our attention to the peculiarities of the
distribution of nonpredaceous benthic invertebrates, the first consumer
link in the detrital food chain.

Ye. P. Turpayeva has shown that the distribution of biocenoses with
predominance of swallowing and gathering animals, in terms of weight, is
positively correlated with the content of fine fractions of bottom
sediments, biocenoses with predominance of "A filterers" are correlated
with the content of middle-sized fractions, biocenoses with predominance
of "B filterers" and "waiters" are correlated with the larger
fractions. Further study of the groupings has involved their spatial
distribution. A. I. Savilov (1961) traced the regularities of their
placement in the Sea of Okhotsk. In separating ecologic groupings, he
utilized information on the sources of food, methods of its capture,

204

degree of mobility of animals and methods of their attachment to the
bottom. The stucjy of the spatial distribution of trophic groupings
required simplification of the classification. M. N. Sokolova (1956,
1960) used only the source of food as a criterion for differentiation of
trophic groupings, and distinguished three groupings: detritophages,
unselectively swallowing the bottom and feeding on buried detritus from
the uppermost layers of the bottom; detritophages which collect detritus
from the surface of the bottom; and sestonophages, which consume
suspended detritus.

The distribution of trophic groupings was found to be directly
related to the mode of sediment accumulation which determines whether
the main portion of the detritus will be suspended in the lowest layers
of water, or precipitated onto the surface of the bottom, or buried in
the bottom. This allowed M. N. Sokolova (1964, 1966) to formulate the
concept of the trophic zone. The trophic zone refers to a section of the
bottom occupied by biocenoses of a single trophic type, i.e., with
predominance (by weight) of a single trophic grouping. The trophic zone
in all its parts is charcterized by similar conditions of feeding for
benthic invertebrates, i.e., by a similar type of distribution of
detritus.

The conditions for predominance of sestonophages arise when the
erosion or transfer of sediment predominates over its precipitation.
Conditions for predominance of detritophages of both groups arise when
the process of precipitation of particles predominates over a given
section of the bottom (Turpayeva, 1954; Sokolova, 1956, 1960).

Analysis of the data on the development of trophic zones on the
shelves of the seas of the USSR, the particle-size composition of bottom
deposits and the content of organic matter in them has allowed us to
reveal the interrelationship between these characteristics. Based on
them, a hydrodynamic regional ization of the Barents, Karsk and Okhotsk
Seas was performed, based on the relationship of areas of the bottom
occupied by various trophic zones (A. P. Kuznetsov, 1970, 1974). It was
found possible to distinguish the types of shelves according to the
predominant type of dynamics of the water, i.e., the fraction of the
bottom area occupied by a given trophic zone (A. P. Kuznetsov, 1974;
Kuznetsov, Neyman, 1975). The following types of shelves were
distinguished: 1) shelves with active dynamics of the waters near the
bottom; 2) shelves with weakened dynamics of the waters near the bottom;
for both types, we can assume that the dynamics of the waters near the
bottom are identical throughout their entire area; 3) shelves where
there is spatial heterogeneity in the distribution of the dynamics of
the waters near the bottom. Shelves of type 1 are narrow and steep,
entirely occupied by zones in which sestonophages predominate. They
include the shelves of the island arcs with clear predominance of
attached sestonophages. In these areas, in places where silty sediment
accumulates, we also find detritophages. Shelves of type 2 are ideally
occupied by a single zone of predominance of detritophages. This type
includes the shelf of Hudson Bay, with its long ice-covered season,
reducing wave mixing, its characteristic bottom configuration and
relatively mild tidal fluctuations of the level. It can be expected
that the reduced dynamics of the waters near the bottom are

205

characteristic for other seas in the Arctic as well. The Baltic Sea, in
which detritophages sharply predominate, is of this same type (A. P.
Kuznetsov, 1963, 1964, 1970, 1974). Shelves of type 3 are shelves on
which, depending on their width and steepness, the direction of
prevailing currents and the distribution of benthic deposits, we find
the corresponding development of zones of predominance of all three
trophic groupings.

Trophic zones which depend on the sedimentation mode are
distributed just a regularly as zones of erosion and accumulation of
sediments. M. N. Sokolova (1960) showed, using the example of the
northwest Pacific, that they most frequently alternate vertically,
following the bottom relief. On convexities of the bathymetric curve,
zones of predominance of sestonophages usually develop; in concavities--
zones of predominance of gatherers, and deeper--swal lowing
detritophages. On the next, deeper, convexity, a zone of predominance
of sestonophages appears once more, etc. Thus, a set of three trophic
zones is placed vertically one above the other.

Shelves differ as to width and steepness (Fig. 10). On all
shelves, the shallows are occupied by sandy or rocky soils, allowing the
development of zones of sestonophages (mobile or attached) in these
areas. Deeper, depending on the width and steepness of the shelf, a
zone of sedimentation is developed to some extent (Gershanovich et al . ,
1974) with predominance of gathering or swallowing detritophages. It
may occupy various areas of the bottom, the predominance of
detritophages may be expressed to varying degrees--from slight
domination (40-50% of the total biomass) to complete domination (over
95%). One regularity is found which has not at present been fully
explained. On broad shelves with a well -developed zone of
sedimentation, the finest clayey silts are dominated by collecting
detritophages, while swallowing detritophages predominate on somewhat
coarser silts. On narrower shelves, where the zone of sedimentation is
not so broad, the very finest silts are dominated, not by collecting,
but rather by swallowing, detritophages (A. P. Kuznetsov, 1963; Neyman,
1963a).

As a rule, the vertical trophic zonality is expressed rather fully
on shelves, which is facilitated by the currents directed along the
edges of the shelf. Sometimes, the influence of the relief on the
distribution of trohic zones may be buried by that of other factors.
For example, if the currents are directed across the shelf, the vertical
trophic zonality may be distorted, to the point of appearance of
spottiness in the distribution of trophic zones (A. P. Kuznetsov,
1970). However, the relationship of distribution of trophic zones with
the mode of sediment accumulation is fully preserved--in these cases,
the zones of erosion and sedimentation are also distributed in spots
(Sokolova, Neyman, 1966).

All of these conclusions were reached in a study of the benthos of
shelves located under subarctic waters. Upon transition to a stuciy of
subtropical and tropical shelves, cases were noted which did not fall
within the system described above. Here, the concept of eutrophic and
oligotrophic types of trophic structures suggested by M. N. Sokolova

206

WO

zeo

300
SOii

fOO
200
300
^00
500

-

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Fig. 10. System of distribution of trophic zones on shelves of varying
widths and steepnesses. Shelf width not drawn to scale. 1,
Sestonophages; 2, Gatherers; 3, Swallowing detritophages.

(1966, 1969, 1972) for the deep water benthos were found to be useful.
A eutrophic structure is formed where the pelagic community is rather
productive and the rate of sediment accumulation is high. These factors
determine the abundant supply of the surface layer of sediment with
organic matter and its rapid burial in a condition suitable for
consumption by detritophages. An oligotrophic benthos structure is
formed where the surface waters are more or less fully stratified, the
pelagic community is low in productivity, the rate of sediment
accumulation is very low. These factors cause the bottom sediment to be
supplied with little organic matter, which is buried in a condition
unsuitable or poorly suitable for utilization by detritophages.

A eutrophic structure results in practically 100% occurrence of
representatives of the three trophic groupings and the appearance of a
zone of dominance of each one under the corresponding conditions of
dynamics of the bottom waters. With a eutrophic structure, the
correlation in distribution of the trophic zones with bottom relief and
the nature of the bottom deposits is quite clearly seen (Fig. Ua). An
oligotrophic structure results in low occurrence of gathering
detritophages, with still lower occurrence of swallowing detritophages;
absence of a trophic zone of swallowing detritophages and weak
development of a zone of gathering detritophages; universal development
of a zone of dominance of sestonophages, depending little on bottom
relief (Fig. lib).

In the first approximation, it can be considered that the factor of
rate of sediment accumulation acts identically throughout the shelf;
therefore, in large-scale regionalization of shelves, we can abstract
ourselves from circumcontinental zonal ity in the mode of sediment
accumulation. On the shelf, only one set of three trophic zones is
usually found (Neyman, 1963b, 1967), so that in large-scale

207

•:x"^^~^^

WM

T^m—

"jjoiuim

y

a

mm

\

K

':'■■'■■/ \ 1 2.

HI-/ \1

\

Fig. 11. Diagram of trophic zonality over a broad, flat shelf under
eutrophic (a) and oligotrophia (b) conditions. Zone of dominance of 1,
Sestonophages; 2, Gatherers; 3, Swallowing detritophages. Not drawn to
scale.

regional ization of the shelves, we can also abstract ourselves from
vertical zonality. The influence of the productive properties of the
shelf waters on the characteristics of the bottom population remains to
be studied.

The first attempt to analyze the trophic structure of the benthos
on the example of the shelves of the eastern portion of the Bering Sea
and the East China Sea (Neyman, 1969b) led to the conclusion of the
decisive influence of the productivity of the waters on the trophic
structure of the benthos. Both of these shelves are broad, flat
shelves, with a well -developed zone of sedimentation in their central
portion. The benthos of the East Bering Sea shelf has a clearly
expressed eutrophic structure, corresponding fully to the high
productivity of the overlying water. The trophic zonality clearly
corresponds to the morphology of the shelf (see Fig. 10a); represen-
tatives of all trophic groups have practically 100% occurrence. On the
shelf of the East China Sea, over broad areas beneath the low-
productivity Kuroshio waters, swallowing detritophages are scarce or
absent (Fig. 12), while gatherers are not represented at all stations,
the zone of predominance of the leading group (<50%); over a large area,
a zone of dominance of sestonophages is found. If we base our judgments
on the distribution of benthic deposits, we would expect the development
of three trophic zones and their distribution according to a type
typical for broad, flat shelves. Thus, on the shelf of the East China
Sea, there is disruption of the trophic zonality, manifested as weak
development of the zone of gatherers and total absence of the zone of
swallowers over large areas of the shelf. All of this fits the
definition of an oligotrophia structure according to M. N. Sokolova.

208

Fig. 12. Distribution of swallowiny
detritophages on the shelf of the
East China Sea. 1, Swallowing
detritophages present in bottom-
digger samples; 2, absent.

This similarity is further increased by the agreement of disruptions in
the trophic structure with the low-productivity Kuroshio waters.

A similar phenomenon was detected on the shelf of the Great Bay of
Australia (Neyman, 1970). This shelf is rather narrow, its main area
occupied by a zone of predominance of sestonophages (see Fig. 10c),
while the zone of gatherers is shifted to the very edge of the shelf.
In terms of morphology and distribution of trophic zones, this shelf is
similar to the shelf of western Kamchatka, where the zone of
predominance of gatherers is also found at the very edge of the shelf,
while the zone of swallowers is shifted to the upper portion of the
slope (Neyman, 1969b). However, on the western Kamchatka shelf, with
predominance of sestonophages (in places they represent 90% of the total
biomass), practically every station brings up significant numbers of
gatherers and swallowers, the biomass of which represents 5-lOX of the
total biomass. In the Great Bay of Australia, gatherers are found at
only 60% of stations, swallowers at 25%, while at 40% of stations,
neither is found. The Great Bay of Australia, like the East China Sea,
contains subtropical waters of low productivity, and here also we see
oligotrophic aspects in the structure of the benthos. However, there
are no disruptions of trophic zonal ity here.

We might think that the oligotrophic structure of the benthos would
be a general property of the benthos of tropical shelf areas. However,
data on the benthos of the shelves of the northern Indian Ocean (Neyman,
1969a) have shown that in areas under productive waters (regardless of
the reasons for the increase in productivity), the structure of the
benthos is eutrophic, while in areas under lean waters, it is
oligotrophic. Data on the benthos of the Bay of Persia (Neyman,
Kondritskiy, 1974) do not fit into this scheme--in spite of the high
productivity of the waters, the benthos of this bay has oligotrophic
features.

Up to now, an oligotrophic benthos structure on shelves has been
detected only where the temperature of the water just above the bottom
remains above 13°C throughout the year. In cold waters, even with a

209

very short vegetation season (and, consequently, low productivity), as
in our own Siberian seas, the benthos has a eutrophic structure (A. P.
Kuznetsov, 1970). We should note yet another fact: In contast to the
abyssal area, where the oligotrophic structure of the benthos is
combined with very low content of organic matter in the bottom deposits
(Sokolova, 1969, 1972), on shelves with varying trophic structure of the
benthic population, no significant differences have been found in the
content of Cq^q in the bottom deposits (Gershanovich et al . , 1974).

In the abyssal zone, the oligotrophic structure is combined with
deep transformations of organic matter (Bordovskiy, 1964). We did not
find analogous data for the shelves. However, since the oligotrophic
structure on the shelves was found only with a water temperature which
remained above 13°C throughout the year, and since the rate of
regeneration of biogenic elements increases by a factor of 10 as the
temperature rises from 5 to 30°C (Maksimova, 1974), we can assume that
with a high temperature, organic matter unsuitable for the nutrition of
detritophages, particularly swal lowers, is present in the bottom
deposits. It might be thought that the reason for the formation of the
oligotrophic structure of the benthos on the shelf is dual --either low
productivity of the shelf waters, or very rapid decomposition of organic
matter. In either case, the supply of the bottom deposits with organic
matter "edible" for detritophagous invertebrates would be reduced,
allowing us to retain the term "oligotrophic" for this structure.
However, the term does not have the same meaning as in the abyssal zone,
either in terms of the reasons of the oligotrophic formation or in terms
of the quantitative indices.

We can draw the general conclusion that for shelves in the
temperate and cold zones, eutrophic structure is characteristic of the
benthos, while in warm waters, depending on the combination of a number
of factors, it may be eutrophic or oligotrophic. For example, along the
east coasts of the oceans, where zones of constant upwelling of water
are found, a benthos with an oligotrophic structure is rare, and is
encountered in limited areas. Along the west coasts of the oceans,
where the low-productivity central waters approach the coastline quite
closely, and in some places even extend onto the shelf, sections with
oligotrophic benthos structure are quite common.

As we compare the peculiarities of the benthos of the shelves,
which are dependent on the mobility of the water and the particle-size
distribution of the bottom deposits, with the peculiarities which depend
on the supply of organic matter in the bottom deposits, we detect the
following regularities.

1. On shelves with active dynamics of the bottom waters,
sestonophages predominate under all conditions. The influence of the
production processes and processes of regeneration of organic matter,
leading to an oligotrophic structure of the benthos, is hardly
noticeable. The trophic zonality characteristic for such shelves under
eutrophic conditions is fully retained. Only the occurrence of
detritophages, particularly swal lowers, changes. They disappear
completely from large areas of the shelf.

210

2. No examples of oligotrophic structure of shelves with weak
hydrodynamics have been found.

3. On shelves with spatially heterogeneous dynamics of the bottom
waters and eutrophic conditions in the zone of sediment accumulation,
zones of predominance of detritophages, swal lowers and gatherers are
formed. Under oligotrophic conditions, detritophages are weakly
developed: In large areas of the bottom they are absent, particularly
swallowers. The zone of predominance of swallowers is not expressed,
the zone of predominance of gatherers is weakly expressed; throughout
almost the entire shelf area, sestonophages predominate. Thus, the
disruption of the trophic zonal ity characteristic of the oligotrophic
abyssal zone is seen on the shelves only under conditions of spatial
heterogeneity of the dynamics of the bottom waters.

The method of separating trophic groupings on the basis of the
source of food has allowed us to approach an interpretation of the
connection between the benthic population and the nature of distribution
and type of transformation of organic matter, i.e., between the fauna of
the benthos and the biogeochemical processes. It has been found that a
similar type of transformation of organic matter causes similar
development and relationship of trophic groupings under conditions quite
different with respect to other characteristics (L. G. Vinogradov, 1963,
1966; Vinogradov, Neyman, 1965). Due to the precise and unambiguous
connection with the conditions of sediment accumulation, trophic zones
and sets of zones are structural units for the description of planetary
regularities of the distribution of the benthic population.

211

5. Communities of Abyssal Macrofauna. (Z. A. Filatova)

The benthic abyssal communities have not been thoroughly studied.
There is a shortage of data on their species composition, geographic
area and conditions of habitation. Very little is currently known about
the physical and chemical conditions on the bottom and near the bottom,
the force and direction of movement of the water above the surface of
the bottom. These data, where available, are scattered and largely
random. In order to explain the peculiarities of distribution and
quantitative predominance of various species of macrofauna on the ocean
floor, it is not sufficient to know the depth of the location, the
nature and distribution of bottom sediments and the macroscopic bottom
relief. We also need information on many other important factors
determining the conditions of life in the bottom layer of water and on
the bottom itself, as well as how they change with time and space.
Nevertheless, using the data which have been accumulated, we can attempt
to imagine the composition and structure of abyssal benthic macrofauna
biocenoses of the ocean, on the example of the best studied eutrophic
zone, that of the northern Pacific. As a first step, let us use the
available, though incomplete, data on the specific composition and
quantitative nature of the biocenoses, and their distribution over the
sea floor.

Deep-water macrobenthic fauna is arbitrarily subdivided into three
dimensional groups. The meiofauna (meiobenthos) measures 0.04-1 mm
(Thiel, 1966, 1975) or 0.5-5 m (Sokolova, 1970), and is the most
massive group of animals. The macrofauna (measuring 5-10 mm) and
megafauna (>1 cm) are the remaining dimensional groups. The nature of
the distribution of these groups of animals on the sea floor is related
to their dimensions: The smaller the organisms, the more evenly they
are distributed on the bottom. Such groups as the small Xenophyophoria,
Tanaidacea, Nematoda or the agglutinating Rhizopoda frequently form a
sort of continuous "carpet" in a number of regions of the eutrophic zone
of the ocean. Therefore, the meiofauna and smaller macrofauna
(primarily the megabenthos juveniles) are most completely accounted for
by the bottom digger. The larger the organisms, the less evenly they
are distributed on the bottom and the more frequently they form various
aggregations, "spots" or accumulations. This is a result both of the
small-scale peculiarities of distribution of conditions of habitation,
and of the nature of breeding and behavior of the larvae and fry.

It is characteristic for deep-water benthic fauna that the species
usually have limited geographic distribution, whereas many genera are
almost cosmopolitan (Hessler, 1974). This is quite important for the
study of the abyssal biocenoses. Studies of the abyssal biocenoses will
yield the greatest results where they are most completely developed,
i.e., in the eutrophic abyssal zones, e.g., in the North Pacific.

212

Before turning to an analysis of the biocenoses of the eutrophic
North Pacific, let us briefly discuss the peculiarities which
distinguish the deep-water (abyssal) biocenoses of the ocean floor from
biocenoses of the shelf zone, and analyze the basic aspects of abyssal
biocenoses of the eutrophic zone of the ocean.

The tremendous size of the abyssal zone biocenoses is one of their
most important specific features. Such factors as depth, bottom relief
and composition of bottom sediment change smoothly in the abyssal zone,
seasonal and diurnal fluctuations in temperature and salinity are
absent, as are tidal movements of the water. Soft sediments
predominate, constant currents are slow. In accordance with this, the
boundaries of the biocenoses are not sharp, and each biocenosis is
large.

A second peculiarity of abyssal biocenoses is the sparsity of
macrofauna and megafauna, in spite of the almost continuous distribution
of the infaunal meiobenthos in the surface layer of the bottom
deposits. This means that the relative quantitative impoverishment of
the bottom fauna is great, since the biomass of the meiofauna does not
compensate for the low biomass of larger animals. The specific variety
of the benthos in the eutrophic zone, however, is rather great.

One peculiarity of the systematic composition of benthic fauna!
biocenoses of the sea floor might be considered a third peculiarity of
abyssal communities. Particularly characteristic are those morphologic
features of organisms which are related to the shortage of calcium at
great depth, the limited food supply, life in total darkness with very
slow movement of the water, in an environment with predominantly soft
sediment and high hydrostatic pressure, influencing the rates of growth
and metabolism, etc. All of this influences the general appearance of
deep water inhabitants; therefore, the abyssal biocenoses differ from
shallow-water biocenoses not only in terms of specific composition, but
also in terms of the general appearance of the component species.

There are a number of species and genera, less frequently families,
which are found only in the abyssal areas, making up the ancient core of
the oceanic complex of benthic fauna. These include the glass sponges
(Triaxonida) , polychaeta from the genera Macellicephala,
Macellicephaloides, Kesun, Jasmineira, Maldanella; bivalve mollusks from
the genera MalletTa, SpirTula, Parayoldiella, Ledella, Vesicomya, a
number of species of Pennatulana, the sea stars Porcellanasteridae, the
Holothurioidea Elpidia, a number of species of the urchins
Pourtalesiidae, and many Pogonophora.

Biocenoses of the lower bathyal and abyssal zones, interconnected
by gradual transitions with increasing depth, are quite characteristic
of the North Pacific. Let us analyze some of these biocenoses, located
in the open portion of the Gulf of Alaska and the waters of the North
Pacific.

The biocenosis Onuphis pallida-Pavonaria pacifica-Ophiophthalamus
normani-Ophiura leptoctema is found in the upper and middle bathyal
region of the Gulf of Alaska. One of its groupings is:

213

Onuphis pall ida-Potamilla symbiotica-Syncoryne sp.-
Ophiophthalamus normani ,~which probably extends from the Gulf of Alaska
along the island slope of the Aleutians and the eastern coast of
Kamchatka to the Sea of Okhotsk. In the Sea of Okhotsk, this is an
independent bathyal -abyssal community, extending over depths of 460-
3314 m on the slopes of the Academy of Sciences sea mount and in the
southern portion of the sea (Ushakov, 1953; Savilov, 1961). In the Gulf
of Alaska, it is encountered at depths of 990-1030 m in clayey silt,
with a bottom temperature of approximately 3.0°C. The total biomass of
the grouping is 5.3 g/m^. One of the leading forms of this grouping is
a clear example of symbiotic adaptation of organisms to life in the soft
bottom at great depths. The hydroid Syncoryne sp. overgrows the long
(up to 50-80 cm) tube of the sedentary polychaete Potamilla symbiotica,
utilizing it as a substrate, while its hydrorhia creates a thick, "
circular weave around the lower end of the tube, holding the polychaete
in the vertical position (Ushakov, 1950; Tendal, 1971). This represents
the "epi fauna of the soft bottoms" in its clearest form. For this
grouping, the large Pavonaria pacifica with Chondractinia, many
Spiochaetopterus polychaetes, Maldanidae (up to 160 indiv./m^, biomass
0.6 g/m^), Melinna ochotica, Travisia pupa, etc., are characteristic, of
the decapod--juveni1e Chionecetes opilio, of the bivalve mollusks--the
large Delectopecten ra'ndolphi, the smaller Nucula cardara, Yoldiella
derjugim and others.

The lower bathyal biocenosis Onuphis pall ida-Yoldia beringiana-
Ophiura leptoctenia is found in the Gulf of Alaska at depths of 1050-
2088 m, over a rather large region from the east slopes of the Aleutian
trough to the traverse of Baranov Island in soft clayey silts; the
temperature at the bottom is 1.9-2.0°C. The total biomass of macrofauna
is from 0.9-57.8 g/m^, averaging 13.9 g/m^. This relatively high
biomass of benthic fauna in the lower bathyal is explained by the
influence of transport of detritus from the highly productive shelf of
the Gulf of Alaska and its accumulation in the lower portion of the
slope and in the upper levels of the abyssal gulf (Kuznetsov et al . ,
1973).

The biocenosis Onuphis pal 1 ida-Yoldia beringiana is typical for the
lower bathyal zone of the Gulf of Alaska. Characteristic for it is the
presence of a number of bathyal forms also present in the Bering Sea.

Onuphis pall ida is a mass form (100% occurrence, more than 100
individuals in a trawl catch). The large bivalve mollusk
Yoldia beringiana is quite characteristic for the biocenosis, although
it is somewhat less frequently found in trawl catches than Q. pal 1 i da
(occurrence 40-50%). This is a typical bathyal form for the" northern
Pacific Ocean and the far eastern seas. Ophiura leptoctenia is also a
common form, occurrence about 60%. It is usually distributed in spots,
within which its quantity in trawl catches may reach 500-1100
individuals.

One peculiarity of the biocenosis is the presence in its
composition of various sea pens (5-6 species, as many as several dozens
of individuals in a trawl catch). They are all characteristic for the
bathyal and upper abyssal Pacific, surrounding its northern portion in a

214

sort of belt. Particularly common are Payonari a paci f i ca (60%
occurrence) and Virgularia cystifera (4'Q-50%). The last species,
together with Protoptilum oriental e. is placed in the group of "coastal
deep-water forms" (Pasternak, 1973). The entire set of these
Pennatularia, elevated above the surface, is considered part of the
"epi fauna of soft bottoms."

Of the irregular urchins, abundantly represented in the next
biocenosis, here we find only Pourtalesia laguncula beringiana, located
in the bathyal of the Sea of Okhotsk and Bering Sea and the northern
part of the Pacific Ocean (A. N. Mironov, 1974).

This biocenosis includes both detritus-collecting forms and
sestonophages and predators. Characteristic are large Actinia (up to 50
individuals in a catch), the brachiopods Friella halli, the large
polychaete Aphrodite talpa, Sternaspis scutata, Terebellide stroemi ,
Brada irenaia, Samythella neglecta, Travisia forbesi , T. pupa,
Augeneria bistnata, etc. Of the small bivalve mollusYs, we find
Delectopecten randolphi (occurrence about 60%), Nucula tenuis, N^.
cardara, Dermatomya sp., Myonera garetti (40%), Malletia truncata, H_.
pacifica, etc. The Echinodermata are represented primarily by a mass of
small Ophiuroidea: 0^. leptoctenia, Ophiophthalamus normani , Ophiolimna
bairdi , as well as Holothurioidea from the Stichopodidae and
Molpadiidae. The large Echiuroidea Prometor grandis and several species
of Pogonophora give this biocenosis an abyssal appearance. It is
therefore intermediate in nature between bathyal and abyssal biocenoses
in this region.

The biocenosis Ophiura bathybia-Malletia cuneata-
Echinocrepis rostrata-Abyssaster tara is encountered in the upper
abyssal of the open portion of the Gulf of Alaska, at depths of 2240-
4740 m. At depths of about 2000 m, it borders with the above-described
biocenosis 0^. pallida-Y. beringiana.

Probably, the biocenosis 0^. bathybia-M. cuneata is also located in
the adjacent portions of the abyssal northeastern part of the ocean. It
is restricted to soft, fine aleuritic and clayey silts, usually with
some pebbles and rounded pumice. The bottom temperature is 0.7-1.6°C,
averaging 0.9°C. The total biomass of the benthos in the biocenosis is
0.5-3.6 g/nr, averaging 1.5 g/m'^. This value is characteristic for the
northern eutrophic zone of the abyssal Pacific. Large silt-eaters are
characteristic for this biocenosis: various irregular urchins and small
Ophiuroidea. Small bivalve mollusks frequently form rather large
populations. The percentage of occurrence of even the leading forms is
low (not over 60%), due to the paucity of macrofauna.

The leading forms are: Ophiura bathybia--dozens or hundreds of
individuals in a trawl catch--and Malletia cuneata--in places up to 30-
40 individuals.

Of the larger forms, various irregular stars (ten species, up to
nine in one station) are important: Echinocrepis rostrata,
Cystocrepis setigera, Urechinus lovem , Echinosigra amphoFa fabrefacta,
Aporocidaris fragills, etc.

215

Quite characteristic for the abyssal northern Pacific are the sea
stars of the family Porcellanasteridae: Eremicaster tenebrarius (up to
15 individuals in a trawl catch), E. pacificus and Abyssaster tara.
Among typical representatives of tRe biocenosis are also
Travisia profundi , Sternaspis scutata, Pennatula phosphorea, etc.

The presence of the large Echiuroidea Prometor grandis is
characteristic for many regions of the northern (particularly the
northwestern) eutrophic portion of the Pacific Ocean; the large
proboscis of these animals extends across the surface of the sediment,
whereas the Echiuroidea themselves are buried in the soft bottom. In
this biocenosis, in addition to P^. grandis, we also see the Echiuroidea
Ikedella achaeta, the sipunculids--Golfingia capitelliformis and G.
birsteini~ The polychaetes, usually so numerous, do not form massive
settlements here: We can note Travisia pupa, Kesun abyssorum,
Onuphis lepta, £. iridescens, etc"! Of the bi valve mollusks,
Malletia truncata, Myonera garetti , Nucula carlottensis,
Delectopecten randolphi, etc., are seen. Four species of "glass"
sponges are seen from the genus Hyalonema, as well as other deep-water
species of sponge--Cladorhiza longispina, Abyssocladia bruuni ,
Polymastia sol pacifica, Bathydorus laevis. The spicules of the
Hyalonema are inhabited by small Actinia, Ceriantharia, Ascidia. and
many Stephanoscyphus. Of the Pennatularia, we find the abyssal
species--Umbe11uia thomsoni and Kophobelemnon stelliferum. Of the
Pantopoda we see HedgpethTaT articulata and Nymphon procerum. The large
Psychropotes and small Myriotrochus and various small Tanaidacea are
seen in small quantities.

The large size of the forms included in the biocenosis 0. bathybia-
M. cuneata, their relatively high population and biomass indicate that
the benthic fauna finds good habitation conditions here and that the
quantity of food on the bottom can support the development of a varied
fauna, particularly collecting and swallowing detritophages.

The biocenosis Spinula oceanica-Eremicaster tenebrarius is purely
abyssal, found in the western and central portions of the North Pacific
at depths of 4660-6010 m on soft, clayey silts. The macrofauna is still
more sparse than in the Gulf of Alaska; in particular, there are almost
no irregular sea urchins, the meiobenthos makes up most of the biomass
of this biocenosis. The leading forms are the bivalve mollusk S^.
oceanica, characteristic for the entire abyssal Pacific and eastern
Indian Oceans, particularly for the northern eutrophic zone, and the sea
star Eremicaster tenebrarius, which, together with E^. pacificus, is also
typical for the abyssal Pacific Ocean.

The total biomass of the benthos is less than 1 g/m^, usually 0.10-
0.15 g/m^ (Filatova, Levenshteyn, 1961). These values of biomass are
characteristic for the boundary portions of the eutrophic zone of the
northern Pacific.

S^. oceanica in places forms mass accumulations, up to several dozen
individuals in a trawl catch. The similar form S^. calcar does not form
massive populations. The sea stars l_. tenebrarius, E. vTcinus,
Abyssaster tara, Vitjazaster djakonovi are typical sTlt-eaters, almost

216

always encountered in numbers of 3-5 individuals per catch. Two or
three species of Gorgonaria and Pennatularia, and small individual
corals Fungi acyathus symmetricus are characteristic. The small
Stephanoscyphus are quite common (up to 15 individuals in a catch, on
concretions or sponge spicules), of the sponges--Polymastia sol
pacifica, Cladorhiza rectangularis, £. longi spina" Of the bivalve
mollusks--the small Acar asperula (on spicules of sponges or the beaks
of squid), Malletia cuneata, various Ledella and Tindaria, of the
polychaeta--Kesun abyssorum, Fauvel i opsi s cFTal 1 engen a , Maldane harai ,
etc. The Sipunculids are rather varied--G"ol fingia vulgaris, G. minuta
(up to 120 individuals in a catch), G^. improvisa, Phascolion pacificum.
Ph. lutense; the Echiuroidea Alomasomabul lata Tup to 40 individuals),
_A. convexa, Ophiura bathybia (up to 235 individuals). Of the irregular
urchins, we find only Echinocrepis rostrata.

The numerous meiobenthos consists of small Tanaidacea, Nematoda,
Foraminifera (primarily agglutinating), juvenile Polychaeta, bivalve
mollusks. Gastropoda, Isopoda, Amphipoda and Ostracoda.

As we move to the south from the relatively productive eutrophic
North Pacific and move away from the coast into the open ocean, the
composition of the biocenoses gradually changes: The significance of
macrofauna decreases, that of meiobenthos increases, and the total
biomass decreases. In the vicinity of 30-20°N, the bottom population
takes on the form which is usual for the oligotrophic zone of the
Pacific Ocean, where the total biomass does not exceed a fraction of a
gram per m^. The remainders of the skeletons of dead macrofauna, nekton
and Radiolaria give the bottom population of these regions a
characteristic appearance and form a substrate for the sparse epifauna--
Stephanoscyphus, small Actinia, etc.

217

7. Trophic Structure of the Deep-Water Benthos.
(M. N. Sokolova) ~

The various size-groups of the deep-water bottom population react
differently to changes in feeding conditions. Therefore, we should
analyze separately the structure of the macrobenthos and meiobenthos.
By meiobenthos, we mean invertebrates measuring 0.5-5 mm. (The minimum
dimension is determined by the size of the apertures in a No. 140
screen, through which the samples are usually washed, while the maximum
is selected arbitrarily.) We consider all organisms larger than 5 mm to
be macrobenthos. The meiobenthos makes up the main portion of the
samples taken by bottom grabs; the macrobenthos, the main portion of the
catch of deep-water trawls. The deep-water macrobenthos is usually
absent in the bottom-grab samples (area 0.25 m^), due to its scarcity,
while the meiobenthos is only partially retained in trawl samples.

The majority of the entire deep-water macrobenthos, and
particularly of the meiobenthos, falls in the deposit- feeding group (see
3.5), i.e., it feeds on the organic matter contained in the sediment.
The invertebrate suspension-feeders consuming suspended (living or dead)
organic matter represent a significant portion of the deep-water
macrobenthos, but are rare in the meiobenthos. The carnivorous
invertebrates, utilizing both living prey and dead animals, are in the
minority in the deep-water free-ranging and sessile macrobenthos but,
apparently, represent the absolute majority of the nektobenthos. They
are in the minority in the meiobenthos.

The trophic structure of the deep-water benthic population, i.e.,
the quantitative ratio (in our studies--by weight) of invertebrates with
various types of feeding experiences significant alterations in the
World Ocean in connection with the changes in feeding conditions for the
dominant trophic group, i.e., for macrobenthic deposit-feeders. The
body sizes of the invertebrate macro- and meiobenthos differ by an
average of a factor of 10, which results from the variation in thickness
of the sediment layer necessary for maintaining of deposit-feeders of
these two size-groups. The requirements of the smaller organisms can be
satisfied with a smaller quantity of food, and therefore they can exist
in a thinner layer of sediment than can the larger organisms.

On the scale of the World Ocean, the greatest changes in thickness
of the surface layer of sediment suitable for feeding of deep-water
deposit-feeders are found at the boundaries of the global zones of
oceanic sedimentogenesis--in connection with the climatic and circum-
continental zonal ity of sediment formation (Bezrukov, 1962; Lisitsyn,
1974).

In general, in the arid zones only the surface film of sediment is
available for the nutrition of deposit-feeders, while in the humid and
equatorial zone--a layer of several centimeters is available, and in

218

pericontinental zones of hemipelagic-type sediment accumulation--tens or
even hundreds of centimeters of surface sediment are available. The
thickness of the surface layer of sediment which can be fed upon by
benthic deposit-feeders is greater, with higher rates of sedimentation
and greater quantities of organic matter reaching the bottom, to be
stored in the sediments in a form which can still be utilized. This
layer is thin where sedimentation rates are low and the quantities of
organic matter reaching the bottom are minimal, where the organic matter
is greatly transformed on the surface of the sediment not being buried
(Bordovskiy, 1964, 1966; Romankevich, 1974, 1975). A sharp decrease in
the thickness of the layer of sediment suitable for nutrition represents
an obstacle to the spreading out of macrobenthic deposit-feeders, more
so than for those of meiobenthos. Consequently, most macrobenthic
deposit- feeders cannot exist in areas with unfavorable oligotrophic
conditions.

Eutrophic conditions are observed in the peripheral and equatorial
parts of the Pacific, Indian and Atlantic Oceans with more or less
significant rates of accumulation of sediment and organic matter.
Oligotrophic conditions are found far from the continents in the open
areas of the oceans with low rates of accumulation of sediment and
organic matter. The locations of these trophic areas in the oceans are
shown in Figs. 13 and 14.

The trophic structure of the macrobenthos changes upon transition
from eutrophic areas to oligotrophic areas, whereas the trophic
structure of the meiobenthos remains unchanged. In areas with eutrophic
conditions, the macrobenthic deposit-feeders are ubiquitous and
predominate over large areas of the bottom, except the peaks of
underwater sea mounts and areas of erosion on their slopes. In areas
with oligotrophic conditions, detritophagous macrobenthos is found
rarely or not at all. The macrobenthos in these areas consists of a few
immobile suspension-feeders and nektobenthic carnivores (Sokolova, 1964,
1969, 1976; Dayton, Hessler, 1972; Shulenberger, Hessler, 1974).
Figures 15 and 16 present examples of the distribution of typical
taxonomical groups of macrobenthic deposit- and suspension-feeders in
the eutrophic and oligotrophic region of the Pacific Ocean. The total
quantity of macrobenthos in the oligotrophic regions is significantly
less than in the eutrophic regions (Table 10).

The meiobenthos, both in eutrophic and in oligotrophic regions,
consists primarily of detritophagous invertebrates. Upon transition
from eutrophic conditions to oligotrophic conditions, the taxonomical
composition (Table 11) and biomass of the meiobenthos become somewhat
poorer (Sokolova, 1970, see also III. 5), but the trophic structure is
not altered (Sokolova, 1969, 1970, 1972, 1976).

Due to this, our analysis of the influence of variations in feeding
conditions on individual feeding groups and the entire trophic stucture
will concern only the macrobenthos.

219

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Fig. 14. niagram of distribution of trophic regions on the Pacific
Ocean Floor. Eutrophic regions: 1, Peripheral pericontinental ; 2,
Peripheral oceanic; 3, Equatorial; 4, Northern and southern oligotrophic
regions; 5, fi, Boundaries of regions (symbols same as in Fig. 13); 7,
Continental slopes and under-water rises; 8, Outer boundary of
accumulative trains (same as in Fig. 13) (not over 300 m deep); 9, Deep-
water trenches (over 6000 m deep).

221

Fit;. 15. niagram of locations of typical groups of deposit-feeders on
the floor of the Pacific Ocean. 1, Sea stars of the family
Porcellanasteridae: 2, Irregular sea urchins; 3, Neither group present
in trawl catches (Sokolova, 1^72).

222

120 140 160 180 160 140 I» 100 80 60 40

Fig. 16. Patterns of distribution of typical groups of suspension-
feeders on the Pacific Ocean floor: 1, sponges; 2, Cirripedia; 3,
Polichaeta of family Serpulidae; 4, None of these groups present in
trawl catches (Sokolova, 1972).

The boundaries between eutrophic regions divide the areas with
similar trophic structure of the population, but with unequally
favorable feeding conditions. These differences are sufficient to limit
the areas of distribution of certain species of deposit-feeders, which
tend toward the boundary separating the eutrophic regions. An example
is the boundary of the pericontinental and oceanic peripheral eutrophic
regions in the Pacific Ocean (see Fig. 14). Near it, the subsurface
reducing zone in the sediment disappears, and the absolute quantity of
organic matter buried in the sediment decreases by a factor of 8
(Skornyakova, Murdmaa, 1976). In the macrobenthos, the frequency of
occurrence of deposit-feeders decreases--Holothurioidea, sea urchins,
stars, Polychaeta, Sipunculoidea, all of which prefer the sediment of
the pericontinental eutrophic region (Sokolova, 1976). The species of
the genera Travi sia and Kesun among the Polychaeta (Levenshteyn, 1970),
Cystocrepis , Fchinocrepis , Helgocystis and Ceratophysa among the
irregular urchins (A. N. Mironov, 1974) do not penetrate into the
organic eutrophic region. These and other similar facts explain the
rather good agreement of the boundaries between trophic areas and
between zoogeographic areas in the abyssal zones (Vinogradova, 1969;
Relyayev et al., 1973; Sokolova, 1969, 1972). Obviously, we see here
the influence of a sharp change in the feeding conditions on the range

223

16

476.R3±in9.49

1660-38.96

11

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of rli stri hution of many species of Heep-water benthic invertebrates,
most of which are deposit-feerlers.

Table 10. Weight characteristics of macrobenthos of eutrophic and
oliqotrophic regions of the Pacific Ocean floor, based on trawl catches,
frame width ?.5 m.

Weight of microbenthos in

No. of trawl catch, q

Trophic areas samples Mean Range

Eutrophi c

Pericontinental

Oceanic

Fquatorial

01 i gotrophic

Northern 7 1.49± 0.39 6.09-0.08

Southern 10 0.39± 0.018 1.06-0.01

Table 11. Frequency of occurrence of basic systematic groups of
meiobenthos {%) and mean biomass of meiobenthos in oliqotrophic and
eutrophic reqions of the Pacific Ocean (Sokolova, 1970).

Oliqotrophic Eutrophic

Group regions regions

Sponqia 33 60

Mematoda 9 7

Polychaeta (family Serpulidae) 5 27

Polychaeta (detritophagous) 19 20

Isopoda - 27

Tanaidacea 24 27

Scaphopoda - 7

Sipunculida - 7

Pryozoa 14 7

Ascidiacea - 7

Mean Biomass, g/m^ 0.007±0.002 0.024±0.004

Number of samples 15 12

224

Vfithin the individual trophic regions, we see medium-scale and
small-scale changes in feeding conditions, resulting from the influence
of bottom topography and hydrodynamics on sedimentation and the content
of organic matter in the sediment. These changes lead to unevenness in
the distribution of the population of deposit-feeders within the range
of distribution of a species.

With various rates of sedimentation, the influence of bottom
topography on the redistribution of nutrient material in the sediment
varies; where the rates are minimal, the influence is least (due to the
paucity of nutrient material). Therefore, in oligotrophic areas the
bottom topography is much less important as a factor changing the
feeding conditions for the macrobenthos than in the eutrophic areas
(Sokolova, 1969). In the eutrophic areas on elevations and protrusions
of the sea floor, the quantity of soft sediment usually decreases as a
result of slower sedimentation or erosion due to greater mobility of the
near-bottom waters (shielding effect); frequently, soft sediments are
totally absent. The accumulation of sediments is observed in
depressions and on flat bottom surfaces (Lisitsyn, 1974). When the
layer of soft sediment is thinned or disappears completely, the
macrobenthic suspension-feeders predominate, while deposit-feeders
become secondary in importance or disappear. When the sediments
accumulate, deposit-feeders predominate. Naturally, changes in the
feeding conditions under the influence of bottom topography are less
significant than changes with replacement of the eutrophic conditions by
oligotrophic conditions.

Within the large-scale forms of bottom topography (continental and
island slopes, underwater mountain ranges, basins of the ocean floor),
we can observe medium-scale variability of the feeding conditions of the
macrobenthos, while within the limits of smaller relief forms (e.g.,
abyssal hills), we see small-scale changes. These large-, medium-, and
small-scale changes in feeding conditions are based on changes in the
accessibility of organic matter in the surface layer of sediment,
necessary for the nutrition of deposit-feeders, correlated to the
thickness of the sediment layer. Under oligotrophic conditions, absence
or an insufficiency of food for deposit-feeders, limiting their
distribution and preventing their dominance in the macrobenthos, is
related to a loss of the nutritive value of organic matter, which is
deeply transformed on the surface of the sediment before it is buried,
while its supply to the bottom is minimal, sedimentation rates as well
as phytoplankton production are lowered. Under eutrophic conditions,
absence or insufficiency of food for deposit-feeders is caused by local
absence of deposits or erosion of soft sediments and the organic matter
they contain when the supply of sedimentary material and organic matter
to the bottom is significant and the production of the phytoplankton is
high.

The concept of the trophic zone, which we introduced (see II 1. 5),
allows us to characterize the trophic structure of the deep-water
macrobenthos in various scales. The medium-scale zonality refers to the
distribution of feeding groups within the limits of the main large forms
of bottom topography, while the small-scale zonality refers to the
limits of medium and smaller forms of relief. Within the limits of the

225

Fiq. 17. Larqe-scale trophic <iines of
deep-water macrobenthos. 1, Latitudinal
eiitrophic zones; 2, Latitudinal
oliqotrophic zones; 3, Periconti nental
eutrophic zone.

large relief forms, as the sedimentation conditions change with depth,
regular alternation of zones of predominance of deposit- and suspension-
feeders is observed, i.e., vertical trophic zonality in the distribution
of feeding groups. In the deep-water macrobenthos, this zonality is
most clearly seen on the slopes of the continents and trenches. The
zones of deposit-feeders here are much larger and more regular than the
zones of suspension-feeders. With the transition from the slopes to the
bottom of the trenches, the vertical trophic zonality, under the
influence of relief, is replaced by a patchy distribution of feeding
groups (Sokolova, 1960, 1964, 1969).

The global trophic zonality of distribution of deep-water
macrobenthos is determined by the distribution of the main productive
zones in the ocean. Two types of zonality are distinguished:
latitudinal (climatic) and ci rcumcontinental . The combination of these
two types of zonality defines the existence of eutrophic and
oligotrophic regions on the ocean floor (see Fig. 13). The latitudinal
trophic zonality of the deep-water macrobenthos consists in an
alternation of gigantic zones of predominance of detritophagous
invertebrates and sestonophagous invertebrates from north to south (Fig.
17). These zones agree approximately with the climatic zones of
sedimentogenesis in the ocean (Lisitsyn, 1974). The two temperate, and
humid equatorial zones of sedimentogenesis generally correspond to the
eutrophic zones of deposit-feeders, the two arid zones--to the northern
and southern oligotrophic zones of suspension-feeders.

The ci rcumcontinental zonality of distribution of feeding groups of
the deep-water macrobenthos consists in the existence of large-scale
eutrophic zones of predominance of deposit-feeders in the

226

pericontinental portions of each ocean. The deep-water eutrophic
pericontinental zones of deposit-feeders occupy the continental and
island slopes, the deep-v"-^-- ■^ ' '"^ *""'
ocean f 1 oor at
zone of depos'

and enriches l..^ ^.-. --. ,-. - - - - -

zones of suspension-feeders, located near the center of the ocean.

227

CHAPTER IV. PRODUCTION OF MARINE COMMUNITIES

1. Primary Production. (0. Y. Koblentz-Mishke, V. I. Vedernikov)

The subject of this section is the primary production of organic
matter in the ocean. It is usually identified with the photosynthesis
of algae, primarily planktonic algae. Actually, primary production
should be identified not only with photosynthesis, but also with all
primary biosynthesis, which consists of photosynthesis and mineral
nutrition. The heterotrophic feeding of phytoplankton, although it
increases the same biomass which is formed in the process of primary
production is, strictly speaking, secondary production. The same
applies also to the heterotrophic feeding of bacteria and to almost all
forms of chemosynthesis, since the source of energy in chemosynthesis
generally consists of the organic compounds or products of their
decomposition, produced earlier in the process of photosynthesis. In
other words, the energy stored in these substances in the form of
chemical bonds is transformed solar energy, absorbed in the process of
photosynthesis.

The study of the primary production of the World Ocean was begun in
the 1920's by the oxygen method, which is not highly sensitive. Some
estimates of the total value of primary production in the marginal seas
were produced by the method of the balance of nutrients. Extensive
development of the study of primary production began in 1951, when E.
Steemann Nielsen introduced the radiocarbon method of its measurement.
For some time, until approximately 1960, intensive collection of data by
routine methods predominated. This descriptive stage was consummated by
the composition of a map of primary production (see Biologiya okeana.
Biologicheskaya struktura okeana [Ocean Biology. The Biologic Structure
of the Ocean]). In the last 15 years, works on physiologic
interpretation of the measured values have predominated, resulting in
some decrease in further collection of large quantities of data. The
physiologic approach to the problems of primary production has resulted
in the use of various, basically biochemical indices and the revision of
the radiocarbon method. At the present time, we see a gap in the
"meeting point" of the results of physiologic works, which in most cases
are performed using cultures of algae, and the results of field
observations. The data produced from cultures are frequently simply
transferred to natural conditions without reservation, although in many
cases there is no sufficient basis for this. In this section, in order
to establish the relationships between the level of primary production,
structural characteristics of phytoplankton and conditions of its
existence, we shall utilize materials obtained under conditions as close
as possible to natural ones. Particular attention shall be given to a
differentiated approach to results obtained in the various regions of
the World Ocean. Comparisons have been made separately for the polar,

228

temperate, and tropical zones and for the oligotrophic, mesotrophic, and
eutrophic communities with primary productions of <100, 100-500, and
>500 mg Z/r\r per day. Sometimes mesotrophic waters are divided into
three types with primary productions of 100-150, 150-250, and 250-500 mg
C/m^ per day. Data for each type of water vary significantly. This
spread of data is caused both by natural fluctuations and by
methodologic errors, particularly biologic errors.

1.1 Methodologic Problems

Let us now discuss methods of measurement of the parameters of
primary production, which have significant influence on the factors
which we shall analyze below. Errors in biologic measurements--of
photosynthesis, concentrations of chlorophyll, and quantities of
phytoplankton--are 1 or 2 orders of magnitude greater than the errors in
measurement of chemical and physical quantities. Furthermore, different
authors use different modifications of methods of biologic measurements,
whereas the physical and chemical methods used d^re generally
standardized.

Primary Production. As a result of many methodologic studies, it
has become clear that the radiocarbon method, in the form in which it
has been used to date, measures the increase only in the biomass of
phytoplankton, as a result of autotrophic fixation of COg- Dissolved
organic matter, synthesized by algae, and the increase in biomass of
phytoplankton resulting from heterotrophic nutrition, are not
measured. The results produced by this method are closer to net
production than to gross production, particularly when there is a
nutrient limitation (Ketchum et al . , 1958).

In determining primary production, a distinction must be made
between measurement techniques, on the one hand, i.e., chemical and
radiochemical approaches to the measurement of the rate of
photosynthesis (production) in each individual sample and the
corrections which have been introduced to the final results, and on the
other hand, the plan of measurement, i.e., the conditions of exposure of
samples and the system of calculations used to consider changes in
production with depth. The simplest and most natural method is the plan
of experiments in situ. Unfortunately, under the complex conditions of
oceanographic expeditions, it is frequently impossible to perform such
measurements. Therefore, a number of plans have been suggested to allow
the measurement of primary production in the water column without
performing investigations. The first was suggested by Steemann Nielsen
(1952): the measurement of photosynthesis in samples taken from various
depths and incubated under conditions of standard illumination. The
second plan, suggested by Yu. I. Sorokin (1956), is based on the
measurement of photosynthesis of phytoplankton in a sample of water from
the surface of the sea, with subsequent introduction of corrections for
changes in its rate with depth. These corrections reflect the
unevenness of vertical distribution of phytoplankton, as well as the
change in the quantity of light energy, necessary for photosynthesis,
with depth, and are determined experimentally. A third plan, which has
become most widely used in recent times, consists in the measurement of
the intensity of photosynthesis in samples brought up from various

229

depths under conditions of natural illumination, reduced by neutral or
selective (blue) filters. The degree of attenuation of light
corresponds to its attenuation in the sea at the depth at which the
samples were taken (samples taken from the surface were exposed to
natural illumination). A fourth plan for determination of primary
production is the "chlorophyll" method of Ryther and Yentsch, and is
essentially the same as the plan of Sorokin. The heterogeneity of the
vertical distribution of phytoplankton is considered by determining the
concentration of chlorophyll, while the correction for light is
introduced using the curve of variation of photosynthesis with light
intensity. The relationship of photosynthesis to concentration of
chlorophyll with optimal illumination (AN^p^) is assumed constant.

All of these plans, naturally, are imperfect. Measurements in situ
most closely reflect the phenomena which occur in nature, and can~5e
used as a standard.

A distinction can be made between random and systematic errors for
the various techniques of measurement. Random errors, based on the
results of the 5?nd voyage of the VITYAZ', amounted to about 20% of the
total deviations of data, resulting from errors in methods and the
natural fluctuations. The relative total deviations increase
exponentially with decreasing production (Fig. 1). With a production of
0.1 mg C/m"^ per day, the total deviation is 100%; this value may be
considered the limit of sensitivity of the method (Koblentz-Mi shke,
1Q61).

AP/P

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Fig. 1. Relative deviations (%) of primary production (P) at the
surface, based on data from the 29th voyage of the VITYAZ' (1), the 46th
voyage of the HUGH SMITH (2) and the 46th voyage of the OSHORO-MARU (3).

230

Of all the systematic errors of the radiocarbon method, the most
important are errors in determination of the stock activity of the
solution and in filtration. Differences in methods of determination of
the stock activity are particularly significant when window- type
counters are used, amounting to 10-20% or even 30% (Jitts, Scott, 1961;
Sorokin, 1963; Steemann Nielsen, 1965). Recently, most researchers have
begun using scintillators; therefore, this source of error has become
less significant.

The basic criticism of the radiocarbon method concerns the loss of
a portion of the synthesized organic matter by filtration, acid
treatment, storage, and drying of filters. Filtration causes a loss of
dissolved assimilates and organic matter formed by Flagellata and other
algae which pass through the filters either whole or in damaged form,
acid treatment results in loss of easily hydrolyzed carbohydrates, while
drying and storage results in loss of volatile compounds such as
volatile acids and ketones. Most numerous are works dedicated to the
losses of dissolved organic matter by filtration. After summarizing the
data of a number of authors, we have come to the conclusion that these
losses, in the surface layer and throughout the entire euphotic layer,
are usually as follows: with primary production of <150 mg Cm'^ per
day— 5-50%: with production of 150-250 mg C/m^ per day— 5-30%; at 250-
500 mg C/m^ per day --20%, at >500 mg C/m^ per day— < 10%.

Pigments. In addition to the primary production determinations,
productivity is frequently evaluated using the data on quantity of
nutrient salts, phytoplankton, the content of suspended matter, ATP or
photosynthetic pigments. The later (usually chlorophyll a) is
particularly frequently used. At the present time, a quantitative
relationship has been obtained between the concentration of chlorophyll
and primary production. It is still more important to note that the
content of pigments allows us to relate the results of determination of
photosynthesis to their quantity, and thus perform the physiological
analysis of the production process.

Determination of pigments in a sample of sea water can be conducted
chromatographically, fluorometrically, or by standard spectrophotometric
methods, the latter being used in most investigations. Its principle
were developed by Richards and Thompson (1952), then further improved
(Parson, Strickland, 1963; SCOR UNESCO, 1966). A comparison of the data
obtained using the formulas of Richards and Thompson (taken as unity)
and derived on the basis of the new specific coefficients of extinction
of chlorophylls, the equations of SCOR UNESCO, and Parsons and
Strickland is presented below.

Author

Chloro-
phyll a

Chloro-
phyll b

Chloro-
phyll c

Richards, Thompson, 1952
Parsons, Strickland, 1963
SCOR UNESCO, 1966

1.00
0.76
0.74

00
05
36

1.00
0.57
0.53

231

Systematic errors of determination of pigments are also based on
incomplete collection of plant material by filtration. In particular,
some of the chlorophyll _a and its derivates pass through the No. 5
membrane filters used in the USSR (Koblentz-Mishke, Konovalov, 1974).
The magnitude of this error has never been estimated, but it is probably
not great, since the filters used by specialists of different countries
produce practically identical results, although their pore diameters are
significantly different (SCOR UNESCO, 1966).

In the lower layers of the euphotic zone, one serious source of
systematic errors, leading to overestimation of the results of
determination of the content of photosynthetically active pigments, may
be the presence in samples of products of the transformation of these
pigments. Upon loss of the central Mg atom, chlorophyll is converted to
phaeophytin, upon loss of phytol--to chlorophyllide and upon loss of
phytol and Mg--to phaeophorbide. The absorption spectra in extracts
practically coincide for chlorophyll a_ and chlorophyllide £ and also for
phaeophytin a and phaeophorbide^ (Holt, Jacobs, 1954; Strickland, 1965;
Lorenzen, 19'67); therefore, standard spectrophotometric methods can
determine only the sum of chlorophyll plus chlorophyllide. If a sample
contains phaeophytin a^ or phaeophorbide a^, calculations by the standard
equations will lead to the overestimation of chlorophyll _a by a quantity
equal to 59% of the content of phaeopigments. Recording of the spectrum
of an extract after acidification (Lorenzen, 1967) allows a correction
to be introduced for the content of phaeopigments but cannot allow
separate determination of chlorophyll and chlorophyllide.

Random errors in the determination of pigments, using the standard
spectrophotometric method, consist basically of errors in the reading of
transmission or extinction spectra.

With the identical concentration of pigments, the accuracy of
determination of chlorophyll a^ is 2-3 times greater than that of
chlorophyll b_ and 4-6 times greater than that of chlorophyll c_. The
shortcomings of the standard method lead in many cases to great errors
in the determination of the content of chlorophyll h_ and chlorophyll _c
in phytoplankton (Strickland, Parsons, 1965; Madgwick, 1966; Wauthy, Le
Bourhis, 1966; Pyrina, Yelizarova, 1971).

Chlorophyll a is the only pigment which is determined with
sufficient reliability by the standard method. If the samples contain
no products of decomposition of chlorophyll a^, parallel measurements of
its content by chromatographic and spectrophotometric methods yield
identical results (Madgwick, 1966). The systematic errors in deter-
mination of chlorophyll ^ by the fluorometric and spectrophotometric
methods usually lead to "overestimation of the results (if phaeopigments
are not determined). The relative random error of determination of this
pigment, as of primary production, increase with a decrease in its
concentration.

Phytoplankton. Data on phytoplankton are required for physiologic
interpretation of the results of determination of primary production.
Of particular significance are data on the biomass (B) of phytoplankton,
expressed as primary production in mg C/m^ (^nhyt^' ^^ ^^^ present

232

time, three methods are used for determination of phytoplankton
carbon: the indirect methods based on ATP (Holm-Hansen, Booth, 1966)
and chlorophyll (Vinberg, 1960; Strickland, 1960), and the direct method
based on microscopic counting of phytoplankton cells and measurement of
their volume, with conversion by equations (Mull in et al . , 1966;
Strathmann, 1967). All three methods are based on coefficients obtained
in cultures. For the conversion from ATP to Cp|^y^, a single coefficient
of 250 is used, regardless of the ecologic conditions (Holm-Hansen,
1969), while the conversion from chlorophyll to ^n\)\/t ^^^^ ^^^
coefficient 30 for cultures and nutrient saturated phytoplankton and
coefficient 60 for light-inhibited and nutrient-deficient phytoplankton
(Strickland, 1960). Obviously, the failure to use differential
coefficients for different ecologic conditions must lead to variations
in the results of the application of these two methods of estimation of
Cp^yt- One shortcoming of the third method is its frequent and
significant undercounting of the number of cells and biomass of
phytoplankton as a result of losses of fragile forms.

1.2 Comparison of Results of Determination of Parameters of
Primary Production at the Surface of the Ocean.

In order to estimate the contribution of systematic errors of the
methods outlined above to ecologic calculations, we have determined the
most probable correlations of production (P), chlorophyll (CI) and cell
number of phytoplankton (N) in pairs for the eutrophic, mesotrophic and
oligotrophic stations (Fig. 2). The best agreement was produced for the
production-phytoplankton relationships. The differences in other
relationships fall within the limits of the standard deviations. The
similar course of the curves obtained directly and calculated on the
basis of the results of two other relationships indicate that the
material used was sufficiently representative.

Conversion coefficients from N to B of phytoplankton (Fig. 3) and
^phyt ^^^^ derived on the basis of a large quantity of material. For
approximate estimates, one can assume that 1 mg of carbon is contained
in 2 million cells of phytoplankton-- the average for various regions of
the World Ocean during various seasons of the year (Koblentz-Mishke,
Vedernikov, 1973). Using these relationships, we can approximately
estimate the specific production (P/B), and, using the equation n =
log(P/B + l)/log 2, we can calculate the rate of cell division n
(assuming that each cell division results in a doubling of the content
of carbon in the daughter cells). Based on the same graphs, we can
calculate the mean content of chlorophyll in the cells of phytoplankton
(Cl/N) and in the biomass (Cl/Cp^y^), the assimilation of carbon by one
cell (P/N), as well as the daily issimilation number (DAN), separately
for the oligotrophic, mesotrophic and eutrophic zones of water (Table 1,
Fig. 4). The indices which are calculated without using the quantity of
phytoplankton agree rather well with the data from the literature,
particularly for the mesotrophic and eutrophic waters. Corrections for
possible systematic errors in the determination of primary production
and chlorophyll have little influence on the equations produced. The
situation is different with the equations whirh include data on cell
count and biomass of phytoplankton, and on the content of carbon in the
phytoplankton. Authors who have determined C-^y^ by various methods

233

i-

S
o

CD

B

10' 10

10^ 10' 10' lo'^ iono=

N, cells/m'

10^ 10" 10^ 10' 10' 10^ 10^- 10^°

N, cells/m^

P, mg C/m^ per day

Fig. 2. Relationships of parameters of primary production at the
surface of the ocean (after B. V. Konavalov): a, primary production (P)
and cell count of phytoplankton (N); b, chlorophyll a_ (CI a) and N; c,
CI a_ and P; 1, regression line produced by direct comparison; 2,
regression line produced by applying the results of two different
graphs; 0, oligotrophic waters; M, merotrophic waters; E, eutrophic
waters.

234

//7^

W

w

w

10'

10'

w

//;'

/o-

Fig. 3. Number of cells per m"^ (abscissa) and biomass (mg/m , ordinate)
of phytoplankton from the Pacific, Indian and Atlantic Oceans.

have obtained rather similar results for
zones, but greatly differing results for
on the results of direct determination of
the rate of cell division and content of
than in mesotrophic and eutrophic waters,
ATP and chlorophyll lead to the opposite
scopic determination of Cp^y^ produces pa
can be assumed that in ollgotrophic water
of 6 times per day (Koblentz-Mishke, Vede
true that Cp^ t/Cl is equal to 0.07 here,
algae contain 15 times as much chlorophyl
phytoplankton consisted of chlorophyll al
approximately 0.7. In actuality, we can
(Steele, 1959; Strickland, 1967). Consid

the eutrophic and mesotrophic
the oligotrophic zones. Based

^Dhvt ^" oligotrophic waters,
chTorophyll in them is higher

whereas calculations based on
conclusion. Direct micro-
radoxical results. Whereas it
s, the cells divide an average
rnikov, 1973), it cannot be

i.e., that the cells of the
1 as carbon. Even if the
one, this ratio would be
assume that it is at least > 4
ering that the overestimation

235

of the concentration of chlorophyll in the oligotrophic waters could
hardly be over 50%, we must assume that Cp^y^ is undervalued by the
counting method by a factor of at least 50 in this case. This
apparently results from underestimation of amount of Flagellata,
Coccoliths and other nanno-forms. These forms, of course, are also lost
during collection and treatment of richer samples, but they represent a
smaller fraction of the cell counts and biomass of the phytoplankton
(Sukhanova, in print; Beers et al., 1975).

The introduction of corrections yields more realistic but also
questionable coefficients (see Table 1).

Table 1. Relationship between basic characteristics of phytoplankton
and its production at the surface.

Oligotrophic Mesotrophic Eutrophic
Item Water Water Water

P v^nrliirl" "i nn

P,

mg

C/m^ • day

1(1.5)
<0.1-10

10(11)
<0. 1-100

50

1-100

Cell count.

N

cells/m-^

2-104
2-103-105

5-106
106-107

109
lOS-lQlO

Biomass Cp^^y^,

, mg

C/m^

0.01(0.5)
0.001-0.05

2.5(5)
0.5-b

500
50-5000

CI , mg/rrr

0.15(0.075)
0.09-0.21

0.25(0.22)
0.15-0.35

5.5

2.5-8.5

P/Cphyt

100(3)
<100-200

4(2.2)
0.2-20

0.1

0.02-0.2

P/N

5-10-5

2-10-6

0.5-10"'^

DAN = P/Cl

7(20)

40(50)

9

Cl/N

7.5-10-6

0.5-10-'^

0.5-10-8

^"■/Cphyt

15(0.15)

0.1(0.045)

0.011

Cphyt/Cl

0.07(6.7)

10(23)

90

NOTE: Numerators show mean values (in parentheses with approximate cor-
rections for systematic errors); denominators show limits of variation.

236

phyt

CI, cr

phyt

Cl/C

10"* 10^ 10^ 10' 10^ 10'

phyt
I, cells/m^

Fig. 4. Comparison of mean values of parameters of productivity and
their relationships for oligotrophia (0), mesotrophic (M), and eutrophic
(E) surface waters of the World Ocean with cell count, N (cells/m-^) ;
B, raw biomass; Cp^y^, biomass expressed as carbon; P, primary
production; P', same, with correction for maximum possible systematic
error; CI, concentration of chlorophyll a; CI', same, with correction;
n, number of divisions per day.

1.3 Environmental Factors Influencing Primary Production

The combination of results obtained in experiments with individual
organisms does not explain fully the occurrence of processes in
communities, since complication of the biologic structure leads to the
appearance of additional properties. Therefore, the basic equations for
primary production as a function of environmental factors must be
derived from the results of observations at sea.

Condi ti ons of i 1 1 umi nati on . Of the factors influencing primary
production in the ocean, the intensity of underwater illumination as a
reason for the variation in photosynthesis has been most thoroughly
studied. Light curves of photosynthesis are constructed for
quantitative description of this variation. Usually, samples from
different levels are exposed under different conditions of illumination
(at sea or in incubators) with parallel determination of the
concentration of chlorophyll. The data produced are used to construct
light curves of the assimilation number (AN). Another method is based
on exposure of aliquots of one sample to various light conditions.

237

The light curves of AN are usually approximated by the formula of
Steele (1962); the position of the optimums on these curves differs
somewhat depending on the method of measurement used (Kabanova et al . ,
1964). The most representative are curves of the assimilation number
obtained in situ, the least representative are the results of
measurement in incubators with neutral filters, since the spectral
composition of the light which penetrates these filters differs
significantly from the spectral composition of the radiation which
penetrates the sea. The optimal illumination (in the photosynthetically
active radiation [PhAR] range) for photosynthesis of phytoplankton in
the upper layers of the euphotic zone in most cases is 0.03-0.15
cal/cm"-10^ lux (Mandelli et al . , 1970; Burkholder et al., 1967). The
absence of light depression under these conditions can be explained to a
significant extent by the good conditions of mineral nutrition and (or)
the dominance of dinoflagellates, which are more resistant to strong
irradiation than are the diatoms, as well as the presence of large
quantities of yellow organic matter, absorbing ultraviolet radiation.
In addition to populations which are resistant to light, populations
have also been found, the photosynthesis of which reaches a maximum at
very low values of irradiation: 0.003-0.015 cal/cm^«min, or 2-10
cal/cm^«day (Koblentz-Mishke et al., 1970; Vedernikov, Solov'yeva,
1972). These value of saturating intensity of light were obtained on
foggy or cloudy days.

The phenomenon of light adaption has been extensively studied in
cultures of algae. As in these cultures, the cells of planktonic algae,
adapted to intensive light and placed to the conditions of saturating
light, manifest higher values of AN than do "shade" cells. It is well
known that the light curves of photosynthesis of phytoplankton living at
various depths differ in terms of the position of the optimums: for
surface phytoplankton, they correspond to higher levels of irradiation
than for deep-water phytoplankton. The difference depends on the degree
of stratification of the water, i.e., the time of adaptation of algae to
specific conditions of illumination.

In a number of regions of the World Ocean, a direct relationship
has been noted between the incident irradiation and irradiation for
which the maximum values of AN are observed. This relationship was
detected in July-August of 1966 over the Kuril -Kamchatka trench in the
Pacific Ocean (Koblentz-Mishke et al . , 1970). It has been shown that
the higher the irradiation at a given station, the higher the value of
irradiation which corresponds to the optimum on the light curve of AN,
determined by experiments in situ. Analogous results were obtained on
expeditions of the Institute of Oceanography, USSr Academy of Sciences,
in the southwestern Atlantic and southeastern Pacific (Vedernikov,
Starodubtsev, 1971; Kabanova et al . , 1974a, b). In the littoral waters
of the Barents Sea in the summer of 1967 a parallel was observed between
incident radiation and the position of the light optimum of the AN
(Vedernikov, Solov'yeva, 1972). The variation found in the Barents Sea
manifests seasonal adaptation, appearing as a sharp drop in the light
optimum in the fall, and a less clearly expressed rapidly occurring
adaptation for cultures and natural populations of marine phytoplankton
(Steemann Nielsen, Hansen, 1959; Menzel , Ryther, 1961b; Ichimura, Aruga,
1964; Krupatkina, 1970). The latter type of adaptation is probably

238

similar to the examples presented above of light adaptation in the
Pacific and Atlantic Oceans. This phenomenon has not been observed for
marine waters, but has been observed in Lake Erie (Verduin, 1956). The
maximum of photosynthesis of phytoplankton in this lake is observed
during the various seasons on sunny days at higher levels of irradiation
than is the case on cloudy days.

Thus, many reported facts indicate that the position of the light
optimum for photosynthesis is related to the conditions of illumination
at the moment of measurement. In contradiction to this, some authors
(Finenko, in print; Aruga, 1965) believe that the light optimum of
photosynthesis of phytoplankton depends primarily on temperature. To
check the correctness of these hypotheses using a single mehod (Yerlov,
1970), data were processed from 77 stations from both domestic and
foreign expeditions, in which the measurements of photosynthesis in situ
were accompanied by optical observations. The values of the light
optima were taken from the light curves of AN obtained at these
stations. They were related to the incident radiation on the date of
measurement (Fig. 5a) and to the temperature at the depth of the optimum
(Fig. 5b). We can see that the position of the optima depends to a
greater extent on incident radiation than on temperature. Thus, the
assumption of rapid alteration of the light optimum for photosynthesis
as a function of weather conditions is confirmed. It is possible that
this alteration is related not so much to adaptation of the
phytoplankton to the level of irradiation present as to the different
depths of penetration of the near ultraviolet, deactivating pigments,
and other peculiarities of the light field. This would explain why, in
highly eutrophic waters, with significant quantities of impurities, the
light optimum for photosynthesis is found at the surface under
conditions of much more intensive illumination than is the case in less
productive waters. It is also possible that light inhibition of
phytoplankton is to some extent an artifact, since during exposure of
bottles, the algae are exposed to inhibiting radiation longer than is
the case in nature, where they can move vertically. It has been found
that in bottles which are moved vertically by ten meters each half hour,
light inhibition of photosynthesis is weaker than in nonmoving
bottles. Still, however, this effect apparently does occur under
natural conditions: we know for instance, (Koblentz-Mishke, 1971) that
the maximum ratio of chlorophylls a:c is present at the depth of the
light optimum of photosynthesis.

The data mentioned earlier, from measurements in situ, were used to
plot generalized light curves of the photosynthesis of phytoplankton
living under various ecologic conditions--for various trophic zones of
the tropical area. The curves are the envelopes of the fields of points
on the graphs relating primary production to level of illumination at
the depth of measurements (Fig. 6a) and standardized curves for the
maximum of photosynthesis (Fig. 6b). The optimal irradiation in the
tropical area is usually between 30 and 100 cal/cm^-day, averaging 70
cal/cm^«day, which amounts to 15-50% of the mean incident PhAR. Quite
different curves are produced for highly eutrophic inshore zones: here
the maximum photosynthesis is observed at the surface of the sea at the
highest values of underwater irradiation observed anywhere under these
ecologic conditions.

239

/C3i

WO

i.n

^ ^ ^ * fi g

^

+ A £i

/^

cal/cn-'day

iKyi>' <?

7^

/J"

i C

Fig. 5. Comparison of energy of irradiation optimal for AN (Eq^), with
incident radiation (Einc) (s) ^nd temperature (t,°C) at optimum depth
(b) : a: 1, optimum An at surface; 2, station with stratified water; 3,
station with mixed water or without hydrologic data; b: 1, optimum AN
at surface; 2, other stations.

C, mg/a

WOO

■}£0 -

■ti-i

t fo

S 1.0

0.1

fj/

a

/^^/

/

i-'

~'-^-.

.^

^

^^

z

1

P,l 1,0 10 IPP JCCP

Fcnecratiag raJlatton, .

al/c:i

• day

Fig. 6. Light curves of photosynthesis of phytoplankton in the tropical
area: a--photosynthesis , mg C/m-^'day; b--same, % of maximum. Abscissa
shows penetrating radiation, ca1/cm^«day. Primary production at
surface, mg C/m^-day: 1, < 2; 2, 2-5; 3, 5-10; 4, 10-100; 5, > 100.

240

As we study the light factor, it is quite important to determine
the effectiveness of the utilization of light energy in the process of
photosynthesis. We know that as one mole of CO2 is fixed into the
products of photosynthesis, 112 kcal of light energy is absorbed, or
9.36 cal/mg C. Expressing the data from measurements of photosynthesis
in energy units and relating them to the quantity of energy available to
plants, we can determine the energetic effectiveness of this process.
The phytocenosis tends toward the upper, naturally, unattainable limit
of this effectiveness during the course of its evolution. The maximum
energy yield of photosynthesis under conditions of scattered long-wave
radiation is not over 27%, while for white light the limit is considered
to be 20%. The maximum quantum effectiveness is estimated as 8-12%
(Rabinovich, 1959). In hydrobiology , the concept of energy
effectiveness of photosynthesis has not yet been established. Of 6
formulas for the calculation of effectiveness (Patten, 1961d) , only one,
in the opinion of Piatt (1969) satisfies the basic requirement of
nondimensional ity :

Q = e"o^ / P^dz,
0

where P, is the photosynthesis at depth z, expressed in cal/m-^, E= is
the light energy striking the surface of the sea (cal/m'^).

This integral effectiveness has been repeatedly estimated by
various authors for various points in the World Ocean (Vinberg, 1960;
Ryther, 1962). According to calculations for waters with various
gradations of primary production, approximately 0.01 to 5% of the
incident light energy is actually utilized in the process of
photosynthesis; the energy effectiveness of photosynthesis of
phytoplankton increases with increasing productivity of a region.

The true effectiveness of photosynthesis in individual samples
taken from various depths VQ^ can be estimated for a layer 1 m thick by
the use of an equation similar to that used in plant physiology:

Q^

Pz

j K p(^)Ez(^)d^

itOO

where E is the penetrating radiation at depth z, cal/m'^;X p is the
index of absorption of light energy by phytoplankton pigments, X is wave
length. We (Koblentz-Mishke et al . , 1975) have estimated the energy
effectiveness Q^ in the equatorial and Peruvian upwel lings of the
Eastern Pacific Ocean. In these areas, Q^ increased from 2% at the
surface to 20% at the depth reached by 1% of the light (Fig. 7).

To calculate Q^ , we must obtain absorption spectra of the
phytoplankton pigments and detailed spectral characteristics of the
penetrating radiation. These measurements have only recently become

241

Ji/'i?

o.ceofOM! o.m s.i i.o /fi.s fpff aaar s.oi ^j ;.o ra.a tan

i C.C!

• •• ■.■■•♦«.'.•,■'. a
•

•

,.j.eio!o.m{}.m a.i u ifj wo h.dci o.ot at ;j fjsm

li'D , ■ ■■ r- — r^'" — : ^, i ■■ ^— ^ '

10

O.J
P. CI

Fig. 7.' Energetic effectiveness of photosynthesis (Q,, abscissa) in
regions with varying levels of primary production at the surface (mg

C/m-^-day): a, < 2; b, 2-10; c, > 10; d, regression lines for graphs a,
b, and c and for data on Q^ obtained during the 17th voyage of the
research vessel AKADEMIK KURCHATOV (17). Ordinate shows light depth (%
of penetrating radiation).

possible, with the appearance of immersible monochromators (Morel, 1973;

Smith, 1973; Pelevin, Kel ' bal ikhanov , 1974)

measurements are not suitable for calculation of Q^ ,

coefficient Q,, i.e., the ratio of photosynthesis to

of light by pigments, water and impurities (a), using the following

equation :

Since previous optical
^■f" 1^^ we have calculated
total attenuation

Ez(l-10-«)

This coefficient Q^ was calculated for the 77 stations we have
mentioned (Fig. 7); its maximum value was found at the lower boundary
of the zone of photosynthesis. The effectiveness of photosynthesis here
averages 10%, at some stations--20%, near its limiting value. Closer to
the surface, Q, decreases in oligotrophic waters more strongly than in
mesotrophic and eutrophic ones. The main reason for this difference is
that in the oligotrophic regions, the water absorbs a greater fraction

242

of the light energy than at the same optical depths in richer regions.
According to our results, in a mesotrophic region, the attenuation of
penetrating radiation by pigments at the surface is 1%, increasing to 5%
of the total attenuation at the depth reached by 1% of the light, while
in a eutrophic region, the corresponding values are 50% and 80%. Thus,
the difference between eutrophic and mesotrophic regions at the surface
is a factor of 50, and at the 1% light-penetration depth--a factor of 16
(Koblentz-Mishke et al., 1975). This is almost proportional to the mean
difference of Q^ in Fig. 7, d: 5.5 times at the surface, 2 times at
the depth of 1% light penetration. These simple calculations confirm
the fact that the light energy absorbed by phytoplankton pigments in
mesotrophic waters is used in photosynthesis with effectiveness equal to
that of eutophic waters.

The values of energetic effectiveness of photosynthesis obtained
indicate that, at least in the lower portion of the euphotic layer, the
radiocarbon method of measurement of primary production yields quite
realistic results. At greater depths, clearly overestimated data are
obtained, apparently a result of methodologic measurement errors.

The possibility of estimating the influence of environmental
factors on photosynthesis by means of energetic effectiveness is also
quite important.

Conditions of mineral nutrition. The study of the variation of
primary production of the oceans with conditions of mineral nutrition is
a significantly more difficult task than the study of its variation with
the influence of light, due to the interconnection and interaction of
the elements of mineral nutrition, due to the fact that in oceanographic
practice their secondary characteristics are determined, and especially
due to the existence in certain cases of feedback between the production
and concentration of nutrients.

The demand of phytoplankton for various nutrient elements has been
studied to widely varying extents. Phosphorus has been comparatively
well studied, silicon to a lesser extent, nitrogen still less,
particularly in the ammonia form, and almost no studies of iron demand
have been made. As concerns the role of microelements and biologically
active substances, the literature contains only a few more or less
probable hypotheses. The primary source of nutrient substances is the
reserve of the substances, which is accumulated in deeper waters as a
result of the decomposition of organisms, then rises into the
photosynthetic layer. A second source of supply of nutrient elements
for algae is their regeneration in the photosynthetic layer itself in
the process of decomposition of organic compounds by bacteria (Dugdale,
Goering, 1967) and by zooplankton. The rate of regeneration of various
nutrients is not identical, and, in general, depends on the temperature
and relationship between the quantities of phytoplankton and
zooplankton. In the tropics, it occurs more rapidly than in the
temperate regions, due to the high temperature and as a result of the
higher relative quantity of zooplankton. A third source is the arrival
of nutrients with river runoff from the land (Sutcliffe, 1972) and upon
mineralization of organic matter in shelf sediment. This source is
important only in the seas and in the inshore areas of the ocean. One

243

important source of nitrogen is the atmosphere. Nitrogen enters the sea
with rain in the form of ammonia and nitrates (Vaccaro, 1965), and is
also fixed by blue-green algae (Carpenter, 1973; Mague et al . , 1974).

It is generally acknowledged (Ketchum et al., 1958) that nitrogen
and phosphorus rise into the layer of photosynthesis in the same ratio
(N:P = 15) that they are found in the phytoplankton. In the photic
layer, due to the different rates of regeneration and loss of these
elements, their ratio varies--nitrogen becomes relatively scarcer than
in the deeper water. The lower the significance of the upward flow in
the supply of alagae with elements of mineral nutrition in comparison to
regeneration of these elements in the photosynthetic layer, the stronger
the depression of the N:P ratio. Therefore, this ratio is a good index
of the degree of limitation of primary production by conditions of
mineral nutrition (Ketchum et al . , 1958; Maksimova, 1973).

Vedernikov (1976a) compared the concentration of nitrates and
phosphates in most regions of the World Ocean (Fig. 8). The N:P ratio
was almost never normal (although if ammonia nitrogen is included in the
analysis, such cases might be more frequent). Furthermore, when the
concentration of nitrates decreased to less than 1 ug -atom ?/ 'i, the
content of phosphates remains at the same level (approximately 0.1-
0.2 ug-atom ? / I) . This level should not lead to extreme phosphorus
"starvation" of marine planktonic algae, since the limiting con-
centrations of phosphates for the growth of cultures are usually < 0.15-
0.55 pg«atom ?/i (Ketchum, 1939; Goldberg et al . , 1951; Strickland,
1965; Thomas, Dodson , 1968). A concentration of nitrates of
< 1 Mg*atom N/z , however, should cause significant nitrogen "starvation
of marine planktonic algae (see Fig. 9).

Analyzing the data on the concentration of dissolved phosphates and
nitrates, we can conclude that nitrogen plays a primary role as the
limiting factor of the existence of marine planktonic algae. Enrichment
experiments performed in various regions have shown that the limiting
elements are most frequently nitrogen, phosphorus and iron, and in
certain cases, silicon and trace elements (Co, Mn , Mo, Zn , Cu).

However, these experiments have shown that the influence of
nutrients is different in short-term and in long-term experiments.
Several hypotheses have been proposed to explain this, but the data
presently available indicate only that long-term enrichment experiments
are more reliable than short-term experiments in determining the
elements which limit production. We can conclude that in most regions
of the World Ocean, nitrogen and, less frequently phosphorus, regulate
the level of primary production. Exceptions are regions of intensive
upwelling, where the main factor limiting production may be the shortage
of forms of iron which can be utilized by the phytoplankton and of trace
elements. In 2-5-day experiments performed in the "juvenile" waters of
upwellings, the addition of iron and trace elements, chelates or their
mixtures led to a significant increase in production (Barber, Ryther,
1969; Barber et al . , 1971). Barber et al . , assume that natural organic
chelators, liberated by the organisms as the surface water "ages," might
be partially responsible for the increase in the growth rate of phyto-
plankton to the north and south of the equator in the eastern Pacific.

244

/Or:

•

/

o

/

+

J

X

«

" o o
o o

00 g

o ^^o'^o 'oo.* "^

i:ifk^=^^-•^

— — Sr-T

X 2

X

+

- - xxx3^ .*

^

X

o •
'x^ o

2- -i!-

+0 O + O/ O OX

/^l?

/r^

N-NO^, ug-atom/i

Fig. 8. Relationship between logarithm of concentration of ni ,rd^es
and phosphates in the surface layer of various regions of the yJjrld
Ocean. 1, Indian Ocean; 2, Pacific; 3, Atlantic; 4, Barents Sea; 5,
line representing N:P = 15.

Some hold the opinion that it is hard to find a better "fertilizer"
than the deep water which rises in the regions of upwelling. However,
the favorable effect of deep water on the photosynthesis of
phytoplankton is not immediately felt, due to the depressing influence
of nonchelated heavy metals, which disappears when this water is held in
darkness.

Enrichment experiments conducted in the southwest Atlantic and in
the Caribbean have shown that the degree of influence of nutrients on
the level of primary production in waters of low productivity in the low
latitudes is several times greater than in highly productive waters in
the higher latitudes (Kabanova, 1972; Kabanova et al . , 1974a, b).

Comparison of level of primary production and conditions of mineral
nutrition. At the present time, it can be considered firmly established
that in most regions of the World Ocean, primary production is limited
by a shortage of the elements of mineral nutrition. On the global
scale, the concentration of nutrients and the level of primary
production change over the water area in a similar manner.

For individual regions of the ocean, the correlation coefficient
between production and the concentration of nutrients has been
calculated. For example, in the northern part of the Indian Ocean, a

245

positive relationship has been found between the mean zonal values of
primary production and the content of phosphates, nitrate nitrogen and
silica in the upper 100-meter layer; the correlation coefficients are
+0.68; +0.83 and +0.88 (Maksimova, 1972). In the more productive waters
of the near-antarctic region of the southwestern Atlantic, the
correlation coefficients between phytoplankton production in the surface
layer and the content of phosphates and nitrates is much lower: +0.42
and +0.44 (Kabanova et al., 1974a ,b).

In regions of low productivity, where the concentration of
nutrients approaches analytic zero, the variation of production with the
content of these elements is difficult to trace due to the significant
measurement errors.

Extensive materials collected in the tropical Pacific, Indian and
Atlantic Oceans were used (Fig. 9a) to compare the concentration of
nitrates and primary production at the surface (> 1300 stations) and at
the depth of maximum AN, i.e., in the layer of optimal illumination (200
stations) (Fig. 9b). The relationship between the values of primary
production and concentration of NO3 is described in log-log coordinates
by an S-shaped curve. Since at low concentrations of nitrogen, its
reduced forms play a significant role in the mineral nutrition of algae
(Thomas, 1970), determination of the concentration of NO2 and NH^ would
result in some straightening of the initial slope of the curve, and it
might be described by the Michael is-Menten equation. The relationship
between the concentrations of nitrate nitrogen and photosynthesis at the
level of optimal illumination is described by practically the same curve
as for the surface.

The effect of nutrients on production can be represented in two
ways. In the opinion of some authors (Fedorov, 1970; Koblentz-Mishke et
al . , 1975), under favorable conditions of mineral nutrition, as a result
of structural changes in the phytoplankton community, a denser
population of phytoplankton exists than in the poorer regions, more
completely absorbing solar energy and using it for more intensive
summary photosynthesis. Other authors (Baslavskaya , 1961; McAllister et
al., 1964; Thomas, Dodson, 1972; Kabanova et al., 1974a ,b) believe that
an improvement in the conditions of mineral nutrition influences
primarily the effectiveness of the action of the photosynthetic
apparatus of each individual cell.

The reality of the first mechanism is beyond doubt. This is
indicated by the positive relationship between the concentration of
nutrients and the abundance of phytoplankton (Semina, Tarkhova, 1970)
and the concentration of chlorophyll (Taniguchi, 1972; our data--Fig.
9c).

The second mechanism has been confirmed by data on the AN under
various conditions of mineral nutrition.

Poor mineral nutrition conditions for phytoplankton may result in a
decrease in the AN: this is shown in enrichment experiments with
natural populations and cultures of planktonic algae. For natural
populations of phytoplankton, inhabiting waters with a high content of

246

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Fig. 9. Relationship of nitrates with production at the surface (a),
production in the layer of maximum AN (b), content of chlorophyll a_ i n
the layer of maximum AN (c), and hourly AN (d): a, b, c, tropics; d,
World Ocean; 1, t° = 0-10°C; 2, t° = 10-20°C; 3, t° = 20-30°C; I,
regression lines; II, Michael is-Menten curves. Vertical line sections
show mean square deviations.

nutrient salts, higher values of AN are characteristic (Saijo, Ichimura,
1960; Aruga, Monsi , 1962; Ichimura, Aruga, 1964; Thomas, 1970; Malone,
1971).

A positive connection has also been established between AN and the
conditions of mineral nutrition in the seasonal aspect (Vedernikov,
Solov'yeva, 1972).

To analyze the variation in values of AN, measured at the optimal
or neaar-optimal level of illumination (AN„p|-) with the content of
nitrates, 370 parallel determinations of chlorophyll _a_, production and
nitrates in various seas and oceans were analyzed. Only the results of
measurement of AN in samples containing 0.1-10 mg/m^^ of chlorophyll _a_
were used, since with lower contents of chlorophyll the random error of

247

determination of AN increases rapidly (Vedernikov, 1973), while with
higher contents, the high population density may have a negative
influence on photosynthetic activity of the phytoplankton .

It was found (Fig. 9d) that for all temperature intervals, there
is a positive connection between the content of nitrates and the values
of AN. As the nitrates increased from the level of analytic zero to 3-5m
g'atom/£, the mean value of AN increased by a factor of 2-3. This
increase was statistically reliable.

Rather high values of AN with practically zero content of nitrate
nitrogen resulted, apparently, from the presence of ammonia nitrogen in

^max

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o

IS

e,Z

aj

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♦4-

t

Ul

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Fig. 10. Maximum energy effectiveness of photosynthesis (Q^^^ %)
and concentration of oxidized forms of nitrogen { pg 'atom/ Ji) for each
station. Stations with primary production of: 1, < 2; 2, 2-10;
3, > 10 mg C/m-^«day.

the water. It is possible that this form of nitrogen and certain dis-
solved organic substances containing the amino group act as a buffer,
preventing the extreme degree of nitrogen starvation of phytoplankton
when the nitrates in the water are completely exhausted (Thomas, 1970).

The relationship between AN^^ and phosphates is weaker than the

relationship with nitrates (Vedernikov, 1976). This confirms once more

that nitrogen limits primary production more strongly than does
phosphorus.

Data on
nutrition ag
regulates th
level of fun
same conclus
maximum valu
of oxidized
layer: the
is positivel
(Fig. 10).

the variation of AN^p^ with the conditions of mineral
ree with the assumption that mineral nutrition not only
e structure of the photocenosis , but also determines the
ctioning of the individual photosynthesizing units. The
ion results from station-by-station comparison of the
es of effectiveness of photosynthesis with the concentration
nitrogen at the same depths--at the bottom of the photic
effectiveness of photosynthesis upon threshold illumination
y related to the concentration of nitrates and nitrites

248

Thus, the conditions of mineral nutrition of phytoplankton
influence production, acting not only on the structure of a community,
but also on the intensity of functioning of the individual organisms.

Temperature. The study of the influence of temperature on the
production characteristics under natural conditions is greatly hindered
by the fact that temperature in nature is positively correlated with
illumination and negatively correlated with the concentration of
nutrient salts and, therefore, influences photosynthesis not only
directly but also indirectly. Also, in determining production by the
radiocarbon method, the effect of temperature may depend not only on the
intensity of photosynthesis, but also on the relationship between
photosynthesis and resoiration, since these two processes cannot be
distinguished by the ^^C method. The close interrelationship of the
temperature factor to light and the effect of nutrients has resulted in
the fact that most authors analyze this factor in combination with the
others.

It has been established that the light adaptation of algae is
closely related to the temperature conditions. Experiments carried out
under semi laboratory conditions have shown that "dark" phytoplankton,
living in the lower portion of the euphotic zone, is adapted to lower
temperatures than "light" phytoplankton. Furthermore, it is thought
that adaptation to low levels of illumination is an apparent phenomenon,
while in actuality the corresponding light curves of photosynthesis are
natural for algae living at low temperatures.

Experiments with both cultures and natural populations have shown
that algae appertaining to various systematic groups differ as to
temperature options of photosynthesis and rates of cell division. A low
temperature optimum is observed in diatoms, a higher optimum in green
algae (Eppley, 1972). The higher the temperature optimum of the algae,
the more intensive its photosynthesis and the higher the rate of
division of which it is capable. The position of the temperature
optimum of photosynthesis and the growth of algae are influenced much
more by temperature conditions of growth and habitat temperature than by
taxonomic composition (Barker, 1935; Braarud, 1961; Ichimura, Aruga,
1964, 1965). Below the temperature optimum, there is a relationship
between the rate of assimilation of COp and the temperature which is
near exponential (Heath, 1972). In cultures of various planktonic algae
grown at 20°C, the ordinary values of temperature coefficient Qj^q = 2-3
are characteristic for broader temperature ranges (20° or 30°C).
However, for narrower temperature ranges (5-10°C), the values of Qiq are
more varied, for example for green algae from 1.3 to 4.8, higher at low
temperatures than at high temperatures (Rabinovich, 1959, page 39).
This apparently results from the fact that in the area of low
temperatures they control the dark reactions which are the main factor
limiting the rate of the entire process of photosynthesis (Heath, 1972,
page 201). At higher temperatures, dark reactions occur more rapidly,
Q^Q decreases, the light energy absorbed by the chloroplasts is not
sufficient for assimilation of additional quantities of CO2, and
photosynthesis begins to be limited by light, even when its intensity is
quite high.

249

The influence of the temperature factor on the photosynthetic
activity of natural populations of phy topi ank ton has been less
studied. The values of Q^q for the phy topi ankton of Japanese lakes and
the Oyashio Current in 10-20°C temperature interval is equal to 2.0
(Ichimura, Aruga, 1959; Ichimura et al . , 1962). It was found without
preliminary adaptation of the algae. After such adaptation, the
temperature coefficient in cultures of certain algae may decrease
significantly--sometimes by a factor of 2 (Steemann Nielsen, Jorgensen,
1968). These authors believe that the reason for this is the great
increase in the quantity of photosynthetic enzymes (per unit of active
pigment and per cell) at low temperatures.

Finenko and Lanskaya (1971), using cultures of the same species,
taken from different latitude zones, showed that algae adapted to low
temperatures decreased the rate of cell division significantly more
slowly as the temperature drops than do the same algae which have
vegetated at higher temperatures.

A comparison of temperature and primary production under optimal
light conditions was conducted on the basis of the data from almost 200
stations in situ in the tropics of the Pacific and Atlantic Oceans
(Fig. llaT. THere is a general tendency toward feedback between the
level of primary production and temperature. This tendency results from
the fact that the temperature is negatively correlated with the
concentration of nutrients: a decrease in the temperature of the
euphotic layer is observed in areas where the deep waters rise. In
zones of different content of nitrates, the temperature has no influence
on production (N-NO3 <1.0 ug*atom/£). Apparently, the temperature, in
and of itself, has no influence on the level of production in the
tropics.

However, analysis of the data of 360 stations in situ in various
latitude areas has shown that the temperature has a"~positive effect on
AN. An analysis was conducted of the relationship of temperature with
AN for marine phy topi ankton inhabiting waters with poor conditions (N-
NO3 <0.1 pg-atom/Ji), moderate conditions (N-NO3 = 0.1-1 ug-atom/Ji) and
good conditions of mineral nutrition (N-NO3 >1.0 yg«atom/A) (Fig. lib).

In all three zones, there is a positive correlation between the
values of AN and temperature. As the temperature rises from 5° to 25°C,
the values of AN increase, with a low content of nitrates, by a factor
of 3.9; with a moderate content of nitrates, the increase is by a factor
of 2.9, and when the nitrate content is high, the increase factor is
2.2; this increase is reliable with a high level of significance. The
curves show that the temperature influences the assimilation activity of
the chlorophyll practically only up to 20°C. The range of 20-30°C can
be considered optimal for the values of AN. At 20-25°C, they are 1.03-
1.13 times higher than at 25-30°C, but the difference between the mean
values of AN at these two levels is not reliable, which is probably
explained by the adaptation of the algae to high temperatures. A
temperature of the surface waters of over 25°C is observed in the
tropics, and in summer in the inshore waters of the temperate
latitudes. Adaptation to this high temperature is apparently possible

250

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— r-. ■*'.'■• . ■ ^ ' "*

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Fig. 11. Primary production (a),
AN (b), and chlorophyll £
concentration (c), and temperature
with various contents of nitrates in
the water: 1, <0.1; 2, 0.1-1.0;
3, >1.0 ug-atom/Ji N-NO3; 4, data on
nitrates not available. Vertical
line segments on graph b show mean
square deviations of AN; a, c,
tropics; b. World Ocean.

in both cases. Thomas (1966) showed that the optimal
the growth rate of the tropical algae Chaetoceros and
in the 27-37°C interval. Williams and Murdoch (1966)
depression of assimilation activity of chlorophyll in
at temperatures of 25-30°C.

temperature for
Nannochloris lies
found no
the summer months

The curves presented in Fig. lib were used to determine the values
of Qj^Q for various temperature intervals (Table 2).

The mean value of Qig for zones with different contents of nitrates
was found to be 2.2 in the 0-20°C interval, 1.7 in the 0-30°C
interval. The former of these values coincided with the value of Q^Q'
obtained for the littoral waters long the Atlantic coast of the USA
(Williams, Murdoch, 1966). From this it follows that for the mean
assimilation activity of chlorophyll under natural conditions over a
broad temperature interval, the most probable values of Qj^q are close to
2, at least in mesotrophic and eutrophic waters. The values of Qig for
individual S'C intervals were maximal at 10-15°C, decreasing rapidly

251

with an increase in temperature, less rapidly with a decrease in
temperature. The decrease in Q-^q with increasing temperature is a
common phenomenon in "sharp" experiments. The slow decrease in AN with
a decrease in temperature apparently results from an adaptive increase
in the content of photosynthetic enzymes in the cells.

Table 2. Values of Q^g for various temperature intervals in waters with
low, medium and high content of nitrates.

Temperature Content of N-NO3, iig«atom/Ji
Interval,

o

C

<0.1 0.1-1.0 >1.0

0- 5 2.2 1.6 1.1

5-10 3.4 2.3 1.5

10-15 3.8 3.9 2.6

15.20 2.1 1.8 1.4

20-25 1.0 1.0 1.0

25-30 1.0 1.0 1.0

0-20 2.7 2.2 1.6

0-30 2.0 1.7 1.4

The decrease in the value of Qiq with improvement of the conditions
of mineral nutrition is notable. It results, first of all, from the
more rapid increase in AN with improvement of the conditions of mineral
nutrition in warm waters in comparison with colder waters and, secondly,
from the higher limiting concentrations of nitrates in these waters (see
Fig. 9d). An analogous relationship between the values of Q^q and the
conditions of mineral nutrition can be obtained upon analysis of the
curves of the variation in the P/B ratio with phosphate content at
various temperatures (Riley et al . , 1949). According to our
calculations, Qiq for the 5-25°C interval is 2.7 with a low content of
phosphates in the water (0.1 pg«atom/£), and 1.6 with a high phosphate
content (0.5 yg«atom/£). These figures are close to those obtained by
us for the 0-20°C interval.

The contradiction between data on the influence of temperature on
photosynthesis and AN becomes clear when we compare the temperature and
concentration of chlorophyll in the tropical portion of the Pacific,
Indian, and Atlantic Oceans (Fig. He). Whereas in the waters with a
concentration of NO3 <1.0 yg'atom/£, the content of chlorophyll
decreases slightly with an increase in temperature, in waters with a
good supply of nitrogen (>1 ug«atom£), it is inversely proportional to
temperature. We find that in regions of the ocean with poor and
moderate conditions of mineral nutrition (NO3 <1.0 uq-atom/i) , the
slight increase in AN with temperature is compensated for by a decrease
in the concentration of chlorophyll, as a result of which production is

252

independent of temperature; in eutrophic regions (N-NO3 >1.0
ug«atom/£), AN increases very slightly with temperature, while the
concentration of chlorophyll decreases rapidly; as a result, a drop is
observed in the level of photosynthesis. In this last case, the
temperature does not influence the rate of photosynthesis directly, but
rather as a factor which is negatively correlated to the concentration
of nutrient salts.

Comparison of results obtained under laboratory and natural
conditio"ns^ In discussing the influence of light on the photosynthesis
of phytoplankton, we should make one general comment concerning the
impossibility of reproducing all of the parameters of the light field in
situ under laboratory conditions. This is particularly true of the top~^
water layer of high irradiation. With "inhibiting" irradiation,
suppression of photosynthesis is usually (but far from always)
observed. With the same irradiation under laboratory or deck-incubator
conditions, the light curves of photosynthesis reach a plateau instead
of descending. We can name four probable causes for the decrease in
photosynthesis beneath the surface of the sea: inactivation of
chlorophyll by excess energy; inhibition of the process by the UV
component of the light field, not considered in measurements of PhAR;
incomplete utilization of the light flux, which is insufficiently
polarized at the surface; and underutil ization of light fluctuating as a
result of the focusing effect of the irregular surface of the sea. The
lack of inhibition of photosynthesis in highly eutrophic water speaks in
favor of UV radiation as the cause of the drop in photosynthesis near
the surface, since these waters contain a yellow substance which absorbs
short-wave radiation.

Thus, the rapid displacement of the position of the light optimum
described above can be explained not only by adaptation of the
phytoplankton, but also by the fact that the energy is underutilized in
the near-surface layers due to certain special properties of the light
field or a combination of this field and the peculiarities of the
pigment system. Illumination conditions may be considered "optimal" at
the depth where this underutil ization stops. If this depth changes only
slightly at a given point in the ocean, different quantities of light
energy will reach the point as the weather changes, leading to a shift
of the optimum on the light curves of photosynthesis. The position of
the "light optimum" of photosynthesis in this case is determined not by
the physiologic peculiarities of the phytoplankton, but rather, by the
parameters of the light field, which explains the slight variation in
the position of the "light optimums" of photosynthesis as a function of
temperature, in comparison to the incident radiation (Fig. 5).

The absolute values of the "light optimums" for photosynthesis,
obtained under natural conditions and in cultures, are basically
similar, exceptions being the data observed in cloudy weather, when the
light optimum of photosynthesis was found to be at much lower
irradiation than is usually observed under laboratory conditions. The
threshold value of irradiation under natural conditions was found to be
related not to the systematic composition of the phytoplankton (as was
indicated in cultures), but rather with the ecologic conditions. If we
consider that at the threshold value of irradiation, the light curves of

253

effectiveness of utilization of sunlight in photosynthesis bend, we find
that its threshold intensity in oligotrophic and mesotrophic regions is
observed at the depth to which <1X of the subsurface radiation
penetrates, in eutrophic waters--about 10%.

Data on the absolute effectiveness of utilization of solar energy
can be used to evaluate the radiocarbon method of measurement of primary
production. The maximum value of this effectiveness is about 20%. This
is the effectiveness which is observed at the bottom of the euphotic
layer. This means that the radiocarbon method, at least in the lower
portion of the layer of photosynthesis, provides quite realistic
results.

A significant portion of the disagreement obtained in the study of
light as a factor in photosynthesis under laboratory and natural
conditions depends on the difference in the spectral composition of the
light. Due to chromatic adaptation, phytoplankton from the lower
portion of the photosynthetic layer has a set of pigments adapted to the
specific spectral composition of the penetrating radiation. This
phytoplankton, when placed in incubators with neutral-density light
filters, absorbs a much lower fraction of the radiant energy than in the
sea at the depth at which it lives. As a result, the threshold of
photosynthesis in incubators is observed at higher levels of irradiation
than jm situ^. The situation is somewhat
filters

are used, but even in this case,
composition of the penetrating radiation
highly productive inshore waters.

improved when blue light
the imitation of the spectral
is imperfect, particularly in

Table 3. Kg (yg-atom N/£) for the rate of uptake of NO3 in cultures and
for the relationship of concentration of oxidized forms of nitrogen to
primary production, concentration of chlorophyll and AN.

Objects studied

Reference

Cultures

Small oceanic diatoms

and coccolithophorids

Neritic diatoms

Neritic dinoflagellates

Small flagellates
Natural populations of

the tropics of the

Pacific, Indian and

Atlantic Oceans

Tropic and temperate
zones of the ocean,

20-30°C

Rate of uptake

0.1- 0.7
0.4- 5.1
3.8-10.3
0.1- 0.4
Relationship of nitrates
to primary production
At surface 3.33
At optimum AN level 2.56
Relationship of nitrates
to chlorophyll at opti-
mum AN level 4.2
Relationship of nitrates
to optimal AN 0.17

Eppley et al

1969

Our data

Vedernikov, 1976b

254

Natural conditions of mineral nutrition are created in laboratories
much more easily than natural light field conditions. The only
exceptions are the peculiarities of nutrition which depend on light.
For example, the rate of absorption of nutients differs under natural
conditions and in incubators. In general terms, there is great
similarity between the specifics of mineral nutition under laboratory
and natural conditions. This is true primarily of nitrogen.

Under laboratory conditions, the relationship of the concentration
of nutrients to the rate of their uptake and growth rate is described by
hyperbolic curves, following the Michael is-Menten equation. The
constant of this equation represented by the symbol K^ is numerically
equal to the concentration of nutrient substances at which the rate of
their uptake or of growth of the algae reaches half of its maximum
value. The value of K^ for these two processes in cultures of marine
diatoms differs slightly. Under natural conditions in the tropics, the
relationship between the concentration of chlorophyll is described by S-
shaped curves, the right parts of which follow the Michaelis-Menten
equation, while the left part is higher, due to underevaluation of
ammonia nitrogen (Fig. 9). We can use the right portion of the curve
to calculate K^ (Table 3). Comparing the values of K3 for cultures and
natural populations, we see that the results produced for AN of natural
populations and the absorption of NO3 by small algae agree well. This
is understandable, since in both cases the population density is
considered in the calculation: K^ in this case represents the rate of
processes in each individual cell or pigment unit. K^ for primary
production and concentration of chlorophyll reflects the integral effect
of the conditions of nitrogen nutrition on the entire phytocenosis.
They have the greatest influence on the concentration of chlorophyll,
while influencing the level of production somewhat less.

These data throw additional light on the problem we have already
discussed, the mechanism of action of the conditions of mineral
nutrition on primary production. The results of determination of the
effectiveness of utilization of solar energy in photosynthesis in
mesotrophic and eutrophic waters have led to the hypothesis that the
primary effect of the conditions of mineral nutrition occurs at the
biocenologic level. Analysis of the relationship of AN with the
conditions of nutrition, however, has indicated that the conditions of
nutrition play a definitive role in the regulation of processes at the
level of the organism as well. However, based on a comparison of K^ for
AN and chlorophyll (see Table 3), we must conclude that this mechanism,
except for regions with very low content of nutrients, is not of great
significance for the development of populations of phy topi ank ton.

No clear relationship has been achieved under natural conditions
between temperature and the production characteristics (except for
AN). However, the results produced indicate that the effective
temperature is manifested at the level of the organism, having no direct
effect at the population level.

255

2. Production of Microflora. (Yu. I. Sorokin)

The microflora of the seas and oceans is represented by
heterotrophic bacteria and fungi (mold, fungi, actinomycetes, yeast).
Among these, the bacteria have the greatest significance from the
standpoint of participation in production and metabolism of the
community. Some researchers also include phytoplankton and
heterotrophic zooflagellata among the marine microflora (Wood, 1965),
but this is ecologically unjustified.

The microflora represent the most important components in the
marine ecosystems (Sorokin, 1971a, 1971b, 1973c). It represents over
60%, usually about 80%, of the total energy flow passing through the
heterotrophic portion of the community, and over 50% of all expenditures
of the community in metabolism (Table 4, Fig. 12).

Considering that the effectiveness factor of biosynthesis (K^) for
bacteria is close to that of aquatic invertebrates--about 0.25--we must
consider that the production of the microbial population is
significantly greater than the total production of protozoa, and all
remaining forms of zooplankton. Therefore, a reliable estimate of
biomass, production and metabolism of the microbial population is a
necessary condition for an accurate ecologic analysis of marine
ecosystems. In this section, we shall study primarily the production
phase, as well as a few problems of the biogeochemical activity of
marine microflora, directly related to the processes of biosynthesis and
destruction.

2.1 Methodologic Problems

In order to determine the productive significance of the microflora
in marine communities, we must determine the characteristics of the
vertical structure of microbial communities and their aggregation;
biomass, production, and metabolic rate of the microbial population;
sources of energy for bacterial biosynthesis; food value of microbes;
contribution of microbes to production, metabolism and transformation of
energy in marine ecosystems.

The production of microflora in bodies of water is determined by
holding freshly taken samples of water in bottles for 12-24 h at the
temperature in situ. The intensity of multiplication of the
bacterioplankton in the bottles is measured on the basis of the increase
in population (comparison of total number of bacteria at the beginning
and at the end of exposure by direct counting) or by measurement of the
intensity of biosynthesis. This is determined primarily by the
radiocarbon method (Sorokin, 1971a, 1973g). The method was offered by
Romanenko (1964) for fresh water. It is based on the existence of an
empirical relationship between the dark assimilation of

256

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257

Plants

phytoplankcon. pbytobcnt 'los . macro;.hvce3
? - 760

Detritus. DOM

Benthlc
Sediment

Kan
(Fishing)

Fig. 12. Diagram of flows of energy (10^^ kcal/yr) in the ecosystem of
the World Ocean. P, production: figures in boxes--consumption by
organisms of the next trophic level; figures in circles--nonassimilated
food; figures in triangles--unconsumed production; DOM = dissolved
organic matter.

COo by heterotrophic bacteria and their production: in bacteria with
different types of metabolism, it varies from 3% to 10%; for
bacterioplankton in sea water it is approximately 5% (Sorokin, 1971a).
Thus, the production of bacterioplankton P can be calculated by the
equation P = 20 A (mg C/m^'day), where A is the daily value of dark
assimilation of CO2, measured by the radiocarbon method (Sorokin,
Kadota, 1972) in water from which the zooplankton and most of the
phytopiankton has been removed by preliminary filtration through a

258

screen of 7-10 m mesh.

This method probably yields somewhat elevated values of production
and respiration of the bacterioplankton (approximately 20-40% high) in
water of the euphotic zone due to the elimination of consumers in the
preliminary filtration, but not due to the so-called "bottle effect."
This effect, described by ZoBell and Anderson (1936) results from the
fact in that when water is stored for a long period of time in small
bottles, intensive growth of heterotrophic bacteria begins. The
intensity of multiplication is higher in small bottles, which is
explained by the adsorption of organic matter onto the walls of the
flasks, making the organic matter more accessible for the microflora.
The observations of ZoBell long served as an argument against the use of
the bottle method for the study of the intensity of bacterial processes
in sea water (Steemann Nielsen, 1972; Banse, 1974); however, these
arguments are based on a misunderstanding. The plate count method used
in the experiments of ZoBell and Anderson considers only a small portion
of the microbial population of the sea water (<0.5%), which reacts more
rapidly than the remainder of the microflora to the death of planktonic
organisms in the samples. However, even for this small portion of the
microbial population, the flask effect appears only after 2 or 3 days of
exposure, whereas the standard exposure of bottled samples for
determination of the production of bacteria and phytoplankton is not
over 1 day. Many experiments have proven that there is no "bottle
effect" in the multiplication of the entire microbial population in
samples of natural water with exposures of up to 5 days at 20-25°C
(Vinberg, Yarovitsyna, 1946; Czeczuga, 1960; Godlevska-Lipova, 1969;
Romanenko, 1969).

There are methods of indirect estimation of bacterial production.
One consists in determination of the time of generation of bacteria on
the basis of the rate of washing of a microbial population out of a
flowthrough cultivator (Jannasch, 1969). If we know the time of
generation of bacteria and their biomass, we can calculate the
production. Another method consists in the determination of the
increase in microflora in an isolated sample on the basis of the change
in the number of particles of a finely dispersed suspension, determined
by means of a Coulter counter (Sheldon et al . , 1973).

The degree of aggregation of marine microflora is determined by

microscopy in a phase-contrast or luminescent microscope (Wood, 1965) or

by the dimensional composition of particles in the suspension,

established by means of a Coulter counter. The method of labeling of

natural bacterioplankton in water samples by small doses of ^^C-labeled
protein hydrolysate, with subsequent filtration on a filter with a pore

diameter of 4-6 um, which retains bacterial clumps, is also used
(Sorokin, 1970b).

In order to establish the sources of energy for bacterial
biosynthesis, we must comparatively evaluate the utilization of
autochthonous and allochthonous organic matter by the microflora. In
analyzing the energetics of a local ecosystem, it is important to obtain
data on the degree of utilization of external dissolved organic matter,
brought in by currents from other regions, since bacterial biomass thus

259

produced (Pg) should be added to the primary production of the community
(P ) to calculate the total energy "input" of the ecosystem (Sorokin,
1971a, 1973c).

The nutrient value of marine microflora for aquatic animals is
estimated by long-term cultivation of these animals, using a suspension
of bacteria as food or by quantitative counting of microflora in the
contents of various segments of the gut (Zhukova, 1954). However, the
basic data on the nutrition of marine invertebrate microflora under
conditions which are close to natural have been obtained in short-term
experiments using bacteria labeled with ^^C or ■^'^P (Marshall, Orr, 1955;
Sorokin, 1966, 1968). The use of -^^P can generate only qualitative
data, since the labeled organic phosphorus in the bacteria is rapidly
involved into the metabolism and is excreted from the organism of the
consumer in the form of inorganic phosphate. The use of ^^C allows
quantitative data to be generated, since ^^C is included into the carbon
chains of the organic matter and is thus much more slowly excreted. The
radiocarbon method can be used to determine the significance of bacteria
in the spectrum of nutrition, to determine the magnitude of food
rations, the assi mi lability of food by consumers, the rates of
filtration and the dependence of intensity of nutrition upon the
concentration of food (Sorokin, 1971a, b,c).

The results of measurement of biomass, production, and metabolism
of a microbial community are expressed in calories under 1 m'^ per day.
A coefficient of 0.92 is used to convert a unit of wet biomass of
bacteria to calories, considering that the content of carbon in
microbial biomass is 10% (Troitskiy, Sorokin, 1967).

2.2 Number, Biomass and Production of PI anktonic Microflora in
Communities with Various Levels of Productivity

In the overwhelming majority of works on marine microbiology, data
were presented on the numbers of saprophytic bacteria growing in protein
media, which gave not the slightest idea of the total microbial
population. The available data, obtained by direct counting and by the
use of ATP, show that the population and biomass of the microbes in the
euphotic zone of unpolluted marine basins averages 1.5-2 times less than
in fresh bodies of water with the same trophic level. This is
apparently the result of the utilization by the microflora in the fresh
waters of significant quantities of allochthonous organic matter
arriving from the land.

Summary data on the mean population and biomass of planktonic
microflora in various biotopes shows that in the euphotic zone of the
eutrophic sea basins--estuaries, shallow bays, lagoons, and also in the
highly productive zones of upwelling, where the primary production
exceeds 1 g C/m^ per day, the total population of bacteria is 1.5-5
million cl/ml, the biomass is 0.5-3 g/m-^ (Melberga, 1968; Karapetyan,
1971; Sorokin, 1971a, c, 1973a; Sorokin et al . , 1975; Fedorov, Sorokin,
1975). Here, as in most marine biotopes, sporeless rod- type bacteria
and micrococci predominate, measuring 0.3-1 x 1-2.5 um. In eutrophic
basins the mean volume of microbial cells is 2 to 4 times greater than
in oligotrophic basins--averaging 0.8-1.5 ym"^.

260

The production of bacterioplankton in warm surface waters of
eutrophic regions averages 0.2-2 g/m-^ per day (according to the data of
the radiocarbon method). The duration of 1 generation (doubling time of
the number of bacteria) is 15-40 h. The mean daily P/B coefficient is
0.5-1. The generation time and P/B coefficients of bacterioplankton as
a whole depend less on the trophic level of the basin than on the
temperature of the water (Sorokin, 1971a, 1973b, 1974; Karapetyan,
1971).

In the upper layer of the water of mesotrophic regions--waters in
the temperate zone, the neritic zone of the tropical and subtropical
regions--the total number of bacteria is 0.3-1.5'10" cl/ml, biomass
0.05-0.5 g/m-^ (Table 5). Production (based on the results of
measurement by the radiocarbon method) in open waters in the summer
averages 0.1-0.3, in the neritic zone--0.3-l g/rtr per day. The P/B
coefficient of bacterioplankton is usually 0.3-0.6.

In oligotrophic surface waters--the trade wind currents in the
oceans and eddy regions--the total number of bacteria decreases to 50-
150-103 cl/ml, the biomass--5-50 mg/m^ (Sorokin, 1964, 1971a, 1973c;
Novozhilova et al . , 1970; Strickland, 1971; Hobbie et al . , 1972).
Production is usually 5-30 mg/m-^ per day, the P/B coefficient is high--
1-2.

In stratified oceanic basins, there are several maxima of
concentration of bacterioplankton: in the surface film, over the
thermocline and in the upper boundary of the intermediate Antarctic
waters. In these layers, the biomass and production of bacterioplankton
are usually several times higher than the average values we have
presented (Sorokin, 1971a, c, 1974) (Fig. 13).

In cross sections from the shore into the ocean, the biomass and
production of bacterioplankton in the surface layer both decrease
rapidly (Fig. 14). The enriching influence of the shelf off small
islands stops at a distance of only a few miles from the shore (Sorokin,
1973b). In the water deeper than the euphotic zone, the population,
biomass and production of bacteria decrease rapidly with depth.
Excluding the layer of the maximum at the upper boundary of the
intermediate Antarctic waters at a depth of 450-550 m, the mean values
of total population of bacteria deeper than 200 m drop to 2-6 • 10-^ cl/ml,
of biomass to 0.2-0.8 mg/m-^, 10-20 times less than at the surface. The
production of bacteria in the deep and intermediate waters decreases
still more— by a factor of 50-100, to 0.01-0.05 mg/m^ per day. In the
layer of the maximum, at a depth of about 500 m, these quantities are 5-
10 times higher (Sorokin, 1971a, c, 1973c, 1974).

These values of number and biomass of bacterioplankton were
obtained by the method of direct microscopy. Measurement of the wet
biomass of bacteria in the deep waters by the ATP method yields 2 to 5
times higher values (Holm-Hansen, 1969; Lyutsarev et al . , 1975). The
reasons for the difference should be sought, apparently, in the fact
that these values of biomass are at the boundary of sensitivity of the
ATP method and cannot be determined by this method with sufficient
reliability. Also, the ATP method yields the actual biomass of all

261

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262

Fig. 13. Vertical distribution of microflora in the Sea of Japan (A),
Black Sea (B), Pacific Ocean in the region of the southern trades ( C) :
1, biomass of bacterioplankton (B, mg C/m-^); 2, daily production (P, mg
C/m^).

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Fig. 14. Distribution of biomass (B, mg/m"^) , daily production (P[^,
mg/m~^) and daily P/B coefficient o1^ bacterioplankton, primary production
of phytoplankton (P-, mg C/m-^ per day) and fraction of aggregates in
bacterioplankton (Ag, %) in a cross section from Heron Island, Great
Barrier Reef, Australia, in the direction of the open sea.

263

living matter, not of bacterioplankton as such. The decrease of biomass
and activity of microflora in the deeper waters of the pelagic zone of
the ocean, indicated by the ATP method, direct counting and assimilation
of labeled COo, coincides with the results of the plate counts of
heterotrophs (ZoBell, 1946) and measurement of the rate of consumption
of ^^C-labeled organic matter by bacterioplankton in samples of deep
water (Sorokin, 1970b; Takahashi , Ichimura, 1971).

One significant peculiarity of marine bacterioplankton is the
clustering of a significant fraction (20-30%) of the microbial cells
into aggregates (Jones, Jannasch, 1959; Sorokin, 1970a; Seki, 1971).
The formation of aggregates measuring more than 5 um in diameter is not
a result of the absorption of bacterial cells on the surface of
suspended particles, but rather a result of the growth of films or
floccules of microcolonies. Their growth is independent of the presence
of suspended particles in the water and continues to occur after
aggregates already formed are filtered out (Sorokin, 1971a). The
formation of organic aggregates under the influence of air bubbles
described by Riley (1963b) does not occur in sterile water (Barber,
1966) and, consequently, is a result of bacterial activity. The
aggregation of bacterioplankton is of important ecologic significance,
since it assures that a significant fraction of the bacterioplankton
will be accessible to coarse filter feeders such as the calanoids, which
dominate in the populations of the pelagic mesozooplankton.

2 . 3 Microflora of the Bottom Sediments

The population density of bacteria in the upper layer of the bottom
sediment varies as a function of the level of productivity of the region
and of depth (Table 5). In the richest sediments of the shelf, the
microflora composes as much as 4-6% of the organic matter in the
sediment. The maximum values of total population, defined by the method
of direct microscopy, is 1-9 -lO^ cl/ml of wet sediment, which was found
in shallow eutrophic regions: the lagoons of atolls, the littoral zones
of inland seas (Butkevich, 1938; Salmanov, 1968; Novozhilova et al . ,
1970; Sorokin, 1970c, 1971b, 1973d). The production of bacteria in the
sediments of such regions amount to 0.2-1 g/1 of wet sediment, the P/B
coefficient is 0.2-0.4. These data indicate the great intensity of the
productive activity of microflora in the sediments of the shelf zone,
assuring their high food value for the benthic invertebrates. It is not
by chance that in this zone, a significant fraction of the benthos
consists of silt swallowers.

In deep-water regions of the inland seas and on the continental
slopes of the temperate and tropical regions of the ocean, the total
number of bacteria in the surface layer of the soil is 0.2-1. 10*10^
cl/ml, their biomass is 0.1-0.4 g/1, their production--5-50 mg/1 per day
(Sorokin, 1964, 1970, 1971c; Anderson, Meadows, 1969; Seki, ZoBell,
1967; Salmanov, 1968; Ernst, 1970). In the bottom sediment in deep-
water areas of the ocean--the radiolarian and pellitic silts and deep-
water clays--the total number of bacteria decreases to 10-50 '10° per ml,
the biomass--to 3-30 mg/1, production--to 0.1-1 mg/1 per day. The P/B
coefficient is quite low--0. 01-0.1.

264

Table 6. Number (N), biomass (B), and production (P) of bacteria in
bottom sediments of the marine basins, per ml of wet silt (Sorokin,
1973c).

Location of Sampling Depth, H, 10^ B (wet P, ug/
Station, Type of m cl/ml weight), ml -day

Sediment pg/ml

Pacific Ocean

Fanning Atoll, coral sand 2 2030 910 226
Majuro Atoll, peri phy ton

on dead coral Z" 6200 2480 2150

Slope opposite Tokyo Bay,

2

2030

3 •"

6200

2725

196

5020

37

5810

14

5330

7

silty-sandy stone 2725 196 94 13
Hear equator, diatom-

radiolaria silt 5020 37 17 1.4

Northern trades, red clay 5810 14 6.6 0.6

Southern trench, red clay 5330 7 3.4 0.03

Sea of Japan

Yamato Bank, al euri tic-

pel i tic silt

70

1.54

175

120.0

West coast shelf, al euri tic

silt

100

0.41

98

4.5

Central trench, aleuritic-

pelitic silt

2000

0.18

25

0.2

Black Sea

Central trench, aleuritic-

pelitic silt

2000

0.98

250

3.2

Slope, al euri tic silt

300

2.96

750

56

180

4.91

2600

48

The distribution of the benthic microflora in the deep-water
regions (Table 6) show that its biomass depends on the level of
productivity of the region (Sorokin, 1970c). These observations
disagree to some extent with the conclusion of independence of the
quantity of suspended organic matter in deep waters of the productivity
of the surface waters (Menzel, 1967). This contradiction may be
explained by the fact that the primary source of organic matter in the
bottom sediment is not dispersed suspended matter, but rather the
remains of planktonic organisms, the number of which is directly
dependent on the level of productivity of the surface waters. These
remains, as well as their faeces, may reach the bottom of the deep ocean
in 5-15 days (Saunders, 1969).

265

2.4 Microflora of Detritus of Peri phy tonic Fouling

Detritus is formed as a result of the destruction of the remains of
dead organisms and the excrement of microflora and protozoa. During the
course of this processing in organic aggregates, which make up the mass
of detritus, a unique type of microcommunity is formed, consisting
mostly of bacteria, infusoria and heterotrophic fl age! lata, as well as
algae (primarily diatoms), and even small Crustacea (Rodina, 1963;
Fenchel , 1970). They determine the food value of the detritus, which
serves as one of the main sources of nutrition of planktonic and benthic
filter feeders, particularly in the highly productive areas of the shelf
and in the water beneath the eutrophic zone (Odum, de la Cruz, 1963).
In "young" detritus particles, the source of energy for bacterial
biosynthesis is the substance of the dead remains itself, while in
"mature" detritus particles, it is the dissolved organic matter of the
sea water (Finenko, Zaika, 1970; Khaylov, 1971). As a result of
bacterial biosynthesis utilizing this external organic matter, the mass
of organic matter in the detritus may increase as it matures, as is
observed, for example, in the feces of shrimp, which was held for
several days in sea water (Johannes, Satomi, 1966).

The total population of bacteria in the detritus and detrital
sediments reaches magnitudes comparable to those of the active silt in
sewage plants: 5-25«10 cl/ml. The mass of bacteria represents as much
as 4% of the total organic matter of the detritus (Rodina, 1963;
Fenchel, 1970, 1972; Sorokin, 1971b; DiSalvo, 1973). The intensity of
the metabolism of detritus (20 mg 02/g'day) is close to that of the
benthic animals of the same weight. Thus, detritus must not be
considered dead organic matter: actually, it is an active component of
the ecosystem. It is the living fraction of the detritus which is
assimilated as it is consumed by filter feeders and sestonophages
(Newell, 1965; Sorokin, 1971b, 1972; Hargrave, 1971; Fenchel, 1972;
Odum, 1975).

The porous surfaces of rocks, dead corals, clastic material, and
particles of large-grained benthic sediment are abundantly overgrown
with periphytonic microflora (Khaylov, Gorbenko, 1967; Sorokin, 1971b,
1973d). The biomass of bacteria in the periphyton on dead coral is 2-5
mg/g of scrapings. A significant portion consists of filamentous forms
of flexi bacteria such as Cladotrix, Crenotrix, or Leucotrix. The latter
frequently cover the surface of dead corals and the periphytonic algae
growing on it in a solid layer. Bacterial foulings on dead corals,
fragments, and large-grained sediment in coral reefs is one of the most
metabolically active components of the ecosystem and the primary
nutrient component of periphyton, consumed by many benthic animals.

2.5 Biogeochemical Activity of Marine Microflora

In aerobic marine basins, the basic biogeochemical functions of the
microflora is the oxidation of organic matter and the creation, by means
of the energy liberated in this process, of their own biomass. The
processes of biochemical consumption of oxygen and formation of CO2,
regulating the content of oxygen, pH and Eh of sea water and sediments
are related to these large-scale biogeochemical processes performed by

266

the microflora; the regeneration of inorganic forms of nitrogen and
phosphorus during the course of oxidation of organic matter by
microflora; the oxidative transformation of ammonia and urea into
nitrates; the fixation of atmospheric nitrogen, achieved by the energy
of oxidation of organic matter; processes of regulation of the content
of dissolved organic matter (DOM) and suspended organic matter in sea
water by the activity of microflora inhabiting the surfaces of suspended
particles (DOM-suspension system); accumulation and precipitation of
biologically active metals (Fe, Mn, Co, certain trace elements) after
they are included into the bacterial biomass and subsequently introduced
into the food chain; the synthesis of organic forms of phosphorus and
nitrogen from inorganic forms upon oxidation of organic matter by the
microflora.

Let us analyze the available data on the intensities and mechanisms
of these processes.

2.6 Intensity of Microbial Decomposition of Organic Matter and
Consumption of Oxygen in the Water and in Sediments

The total concentration of organic matter in the water of the ocean
is 1.5-2.5 mg C/1, or about 15 kg/m^ of dry organic matter. About 60%
of this matter is represented by the relatively stable fraction of
aqueous humus (Skopintsev, 1966; Ogura, 1972), the remainder--by low-
molecular components: amino acids, fatty acids, carbohydrates (Duursma,
1965; Khaylov, 1971; Andrews, Williams, 1971). The absolute content of
organic matter, its composition, the content of the available fraction
of DOM and suspended matter, determined by the potential BOD
(biochemical oxygen demand) or the potential production of bacteria
(Fig. 15), change relatively little right up to very great depths
(Novoselov, 1962; P. M. Williams, 1969; Starikova, Korzhikova, 1970;
Finenko, Ostapenya, 1971; Sorokin, 1971a, d,g; Menzel , 1978). These data
contradict the traditional concept of the predominance of inert aqueous
humus at great depths, which was set forth at one time to explain the
extremely low BOD in the deep waters of the ocean. It was based on the
concept that the source of replenishment of organic matter in the deep
water consists of the remains and excrement of the plankton sinking down
from the higher layers.

According to modern concepts, the deep and intermediate waters are
formed of productive surface waters descending at the convergences in
the high latitudes, then drifting in the direction of the equator. In
the zones of the tropical divergences, they rise and are redistributed
by the equatorial currents (Stommel, Aarons, 1960; Veronis, 1972). In
accordance with this model, the main path of penetration of organic
matter into the deep and intermediate waters is its horizontal transfer
from the productive high-latitude regions (Redfield, 1942; Wyrtki,
1962). This mechanism explains fully a relative uniformity of
distribution of organic matter in the water column described earlier.
The low actual values of BOD are explained not by the great stability of
organic matter in the deep waters (which has not been confirmed by
recent studies), but rather by the unfavorable conditions for the
functioning of deep-water microflora; the joint inhibiting effect of low
temperature and high pressure (Sorokin, 1969, 1971c; Jannasch et al . ,

267

t

^^.2

C.// ffj

iJ.S IfC

0
1

S
1 —

//

/8 rs

SCO h7:j pp

Fig. 15. Vertical distribution of organic matter (DOM) in the water of
the Western Pacific: CD, total content of DOM (mg C/1); CS, organic
carbon in suspension (pg/l); DC, dissolved carbon ( iig C/1), data of Ye.
A. Romankevich; PP, potential production of bacteria (mg C/m-^) .

2 ^/ s 6 /o ;z ///
—Exposure, days
Fig. 16. Rate of assimilation by bacterioplankton (4°N, 135°W) of the
labeled protein hydrolysate injected into a sample of sea water at
moment of closing of a water bottle at 4000 m depth after its subsequent
exposure at this depth for 7 days (1), then in the laboratory at 2°C (2)
and on the deck at 30°C (3). Initial concentration of hydrolysate in
samples 0.3 mg/1 , initial radioactivity .2 10" pulses/1. R =
radioactivity of bacterioplankton, 10^ pulses/100 ml.

268

waters at depths of 400-800 m, the values of destruction,
to ^^C and ATP data, increase to 3-5, in the layer of the

1971). Experiments have shown that the bacterial activity in deep

samples (from 3000-4000 m) upon exposure of the samples in situ, is low

even when the samples are enriched with easily assimilated organic
matter (Fig. 16).

The rate of biochemical decomposition (respiration) in deep waters,
expressed in units of oxygen consumed, according to the results of
physical and chemical calculations (Riley, 1951; Munk , 1966; Arons ,
Stommel , 1967) and measurements of the concentration of ATP and ETS
(electron transport enzymes) in the plankton yield values of
decomposition in deep waters of 0.01-0.06 mg 02/m per day (Strickland,
1971; Hobbie et al . , 1972). This rate of destruction corresponds to an
oxygen consumption of 0.1-0.2 mg/1 yr. With this rate of destruction,
the reserve of oxygen in descending Antarctic waters should be
sufficient for 50-100 years.

Direct analyses of the intensity of the destruction in the "old"
deep waters in the central part of the Pacific by the -^ C method have
yielded quantities close to the calculated quantities (Table 7). In the
deep waters of the Western Pacific, where, according to the model of
global circulation (Kuo, Veronis, 1970) the primary flow of meridional
advection of Antarctic water occurs, the values were 3 to 6 times higher
(Sorokin, 1971a). In the upper layer of the intermediate Antarctic

according
^e bacterial

maximum at a depth of 500-550 m- to 10-20 mg 02/m-^ per day. With this
intensity of destruction, we should see a shortage of oxygen at this
level within 1-2 years, which does actually occur (Fig. 17). These data
indicate that the shortage of oxygen ordinarily observed in intermediate
waters is formed primarily as a result of local consumption of O2 by
microflora which have a constant maximum of activity here.

The rate of decomposition in the surface waters of the pelagic zone
of the oceans is 20-30 mg 02/m-^ per day in oligotrophic waters, 50-200
mg 02/m'^ per day in mesotrophic and eutrophic waters.

Determination of the potential destruction (long-term exposure of
samples at 20-30°C) by the ^'^C and BOD methods yield values of 0.15 mg
O2/I , both in deep and in surface samples (Sorokin, 1971a, 1973c;
Novoselov, 1962). The BOD rate constant in surface waters of the ocean
is 0.02-0.10, close to the constant of the rate of destruction of
phytoplankton in sea water (Skopintsev, 1966; Finenko, Ostapenya, 1971;
Ogura, 1972).

The rate of bacterial destruction of organic matter in the bottom
sediments of the seas can also be characterized by the rate of oxygen
consumption, since biologic oxidation of organic matter in sediment,
performed primarily by microflora, significantly predominates over
chemical oxidation. The rate of destruction of organic matter in bottom
deposits, based on averaged data for various biotopes and the integral
values of destruction beneath each square meter in a layer 5 cm thick
(considering the nature of distribution of bacterial activity in the
sediment) are presented in Table 8. In the sediment of the neritic
zone, 1 g of silt absorbs about 0.1 mg 02/day. The annual destruction

269

Table 7. Mean biochemical oxygen demand (BOD, mg Op/m per day) in waters

of the ocean, and as determined by various methods (Riley, 1951; Novoselov,

1962; Munk, 1966; Arons, Stommel , 1967; Pomeroy, Johannes, 1968; Holm-

Hansen, 1969; Sorokin, 1971a, Ostapenya, 1971; Strickland, 1971, and
others) .

Biotope

Temperature

Method

Other methods*

Subarctic surface water
Shelf water from boreal

zone
Surface water of boreal

zone
Tropical water of coral

shoals
Tropical surface water

of coastal upwelling
Tropical surface water

of equatorial divergence
Tropical surface water

of western pelagic zone
Tropical surface water

of central ocean
Intermediate Antarctic

water of central ocean
Deep water of western part

of ocean
Deep water of central

region of ocean

1-3

--

4

(b)

18

250

300

(b)

16

80

100

(b)

30

200

400

(b)

19

150

240

(ATP), 190 (b)

25

70

50

(ATP), 60 (b)

28

25

70

(b, BOD)

27

20

40

(b, BOD)

6-8

5

3

(ATP, b)

2-4

0.3

0.3

(b)

2-4

0.4

0.2
0.1

(ATP, TP),
(b, TG)

*Methods: b = measurement of oxygen consumption in bottles in short-term
or long-term experiments; ATP = calculation on the basis of the content of
ATP in plankton using the ratio BOD:ATP = 500; TP = theoretical calculation
on the basis of physical data; TG = theoretical calculation on the basis of
geochemical data.

in these sediments is about 200 g 02/m^. The oxygen shortage caused by
this intensive consumption in the sediment of the neritic zone is largely
compensated for by its liberation upon photosynthesis by the peri phy ton and
phytobenthos. Due to the intensive destruction occurring in the bottom
sediments in the neritic zone and shelf, about 20% of the total primary
production is decomposed by the bottom microflora.

The bottom sediments of the slopes are also characterized by rather
intensive metabolism of their microflora: up to 40 yg Op/day, or 30-60 g
02/g of sediment. The intensive metabolism of the microflora in the
sediment on the slopes is a result of the high rates of sediments
accumulation and the rapid delivery of fresh organic matter from the shelf
as the upper layer of sediment flows down the slope.

270

O O

i>-» u-i CO

O O O

O ir. -T

CM .-I I

U fj-i u o

3 il *J D. O

c a O C, l-r 2
L" -3 n 3 CJ -.-(

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•J ^-^

271

to

zo t, c

0 Z5 50 75 0^

0 fS ID .'J VD .5C 5P Bb, ?b

2C3-

^ffff

'SPO

c

o

. -.^■^.}_L'f- _ .*■.'-'

St^ff--,

mo-\'

?.5 /.p /.5 n^c

zoo a, PP

Fig. 17
factors

or 07°

Vertical distribution of bacterioplankton and environmental

in the region of the equatorial divergence in the eastern Pacific

(01°S. 97°W) . Bb and Pb = biomass and daily production of bacteria
3\

(mg/nr^); a - relative activity of heterotrophic bacteria; PP - potential
production of bacteria (mg/m-^); DOC - dissolved organic carbon (mg C/1);

0

2 - dissolved oxygen (% of saturation); t, C - temperature,

In deep-water sediments of the pelagic zone, the intensity of^
destruction decreases by 2 orders of magnitude, to 0.2-0.5 iig 02/m^. Only
about 0.3% of the primary production of pelagic zone is destroyed in these
sediments.

Calculations on the basis of data on the total destruction of organic
matter in benthic sediment of the ocean yields a value of 1.6 10^ t of
carbon, or about 6% of the global primary production. This level of global
primary production is based on studies by the radiocarbon method, but if we
consider that the value produced by this method is probably low by a factor
of 3 or 4, the actual fraction of primary production which is destroyed in
the benthic sediment should be estimated as 1.5-2%.

Data on the intensity of bacterial production and destruction, the
coefficients of specific production of marine microflora and the variation
in the intensity of metabolism with temperature in situ (Sorokin, 1969,
1970d,e, 1971a, g, 1973c, d) allow calculation of the approximate total
values of destruction of organic matter, bacterial biomass and production

272

in the ocean (Table 9). In the calculations, we used the relationship
between daily bacterial production (P, mg C/rn^) and destruction (D, mg
02/ni^): P = 0.08 D (Sorokin, Kadota, 1972). The total bacterial
production of organic matter in the World Ocean is over 2 •10^'^ t of carbon
with a total biomass of the microflora of 0.23-10^ t. The predominant part
of bacterial production (over 60%) is created in the warm surface waters
between 20° N and 20° S at 20°-28°C. This explains the relatively high
mean daily P/B coefficient for the microflora of the World 0cean--0.35.

In the high latitudes, bacterial processes in the organic matter cycle
are inhibited by the low water temperature. Only about 2% of the total
bacterial production is created in these waters. The bacterial production
and, consequently, destruction of organic matter in the benthic sediment
represents only about 1.5% of their values in the water, since most of the
ocean floor (over 80%) consists of deep-water sediment with little content
of organic matter, where the metabolism of the microflora is inhibited by
the high pressure and low temperature.

The total annual destruction of organic matter in the World Ocean is
near 2.5*10^^ t Oo, or S'lO^*^ t carbon (respiratory coefficient 1.2). This
quantity in principle should be close to the primary production of organic
matter by microflora. However, a comparison of this quantity with the
primary production in the World Ocean, based on theoretical calculated
values of oxygen consumption (Skopintsev, 1967) or measurements by the
radiocarbon method (Koblentz-Mishke et al.,1968) shows that consumption is
only one-third of the values of destruction presented above. This
disagreement is most probably a result of the generally recognized fact
that the values of primary production determined by the radiocarbon method
is underestimated (Arthur, Rigler, 1967; Pomeroy, Johannes, 1968; Riley,
1972).

All of the errors of the radiocarbon method lead to lowering of the
results (Sorokin, 1971a). These errors were particularly great during the
first few years of application of the method (before 1960). The values
produced at that time formed the basis for calculations of the total
primary production of the World Ocean presently used for global estimates
of productivity (Moiseyev, 1969; Ryther, 1969; Bogorov, 1974).

Calculation of the probable energy losses in the heterotrophic portion
of the living population of the World Ocean indicate a necessary energy
"input" to the ecosystem of 7.6'10^' kcal/yr which is also three times the
calculated value of primary production.

2.7 Participation of Microorganisms in the Cycling of Nutrients

The decomposition of organic matter by microflora and production due
to the energy liberated in this process of bacterial biomass represent one
of the basic mechanisms of the circulation of nitrogen and phosphorus in
the sea. In the process of microbial decomposition the nutrients are
regenerated. A great significance of biogeochemical regeneration of
nutients results from the fact that photosynthesizing plants can consume
largely their inorganic forms. Therefore, the rate of regeneration and of
their transfer from zones of regeneration to the euphotic layer is a
primary factor regulating the productivity of the oceans. The rate of

273

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274

regeneration, on the average, is proportional to the indices of destruction
rate, such as the BOD (Redfield et a1., 1963). Microorganisms have no
monopoly on the regeneration of nutrients. Other heterotrophs also take
part in the destruction of organic matter. Their share in this process
generally corresponds to the share of their participation in the
destruction of organic matter, or the fraction of the total energy flow
which they expend. There are rather stable relationships between the
respiration of zooplankton and the quantity of mineral forms of nutrients
which they liberate: they average 80 for phosphorus, 20 for nitrogen
(Conover, Corner, 1968). These values in this case are significantly lower
than the stoichiometric relationships with total oxidation of matter by
phytoplankton, which is related to the selective assimilation of nutrient
enriched substances and their incomplete oxidation by zooplankton. During
bacterial oxidation of organic matter in sea water which is poor in
nitrogen and phosphorus, these relationships may also be lower than the
stoichiometric values, particularly since a significant portion of the
nutrients is consumed by the bacteria themselves for biosynthesis. The
consumption of inorganic nutrients by bacterioplankton in some biotopes
makes the bacterioplankton a serious competitor for the phytoplankton.
This occurs in surface tropical waters where, even within the euphotic
zone, most of the inorganic phosphate is consumed by bacteria, but not by
phytoplankton (Sorokin, Vyshkvartsev, 1974), since the microflora oxidizes
primarily "old" organic matter, brought in from other regions of the ocean,
which is poor in phosphorus.

The most important function of the microflora in the cycle of
nutrients is that they can mineralize or assimilate biogens in such stable
dissolved organic compounds as nucleic acids. In a number of biotopes, for
example, in the surface tropical waters, the main stock of nutrients is in
just these forms. Their inclusion in the metabolism of the plankton
community can occur only through the process of biosynthesis of the
bacterial biomass, which is then mineralized by the bacteria-consuming
planktonic animals, primarily the ciliates and phytophagous Copepoda. It
has been established that the ciliate, in a period of 5-15 minutes,
liberate a quantity of mineral phosphate equal to its total content in the
body. For the calanoids, this time is 5-10 days. The Protozoa, in spite
of their relatively low biomass, apparently play a leading role in the
mineralization of the biogens in the organic matter of the bacteria and
phytoplankton (Johannes, 1964, 1968), since the Protozoa perform a
significant fraction of the total metabolism of the community (see Fig.
12).

Studies of the vertical distribution of nitrates and phosphates, the
content of organic phosphorus, O2 and CO2 in various regions of the ocean,
have revealed regular changes in the relationship of their concentrations,
which develop in the course of mineralization of the organic matter of the
phytoplankton. Thus, the atomic ratio of nitrates to phosphates in the top
300 m of water is close to that in the cells of the phytoplankton--15:l
(Redfield et al . , 1963). It has still not been established with certainty
just where the processes of mineralization are located in the waters of the
ocean (Menzel , 1970). The assumption which was earlier held, that
processes of mineralization and related formation of the oxygen minimum
occurred due to utilization of locally produced organic suspended matter,
cannot explain the regularities of quasi-conservative distribution of

275

phosphates and dissolved oxygen in the water which have been observed.
Their distribution is related not only to local processes of
mineralization, but also to the global oceanic circulation. The most
acceptable solution is the assumption that processes of mineralization,
leading to the generation of mineral phosphate and the formation of the
oxygen minimum, occur in the intermediate Antarctic waters along the path
from the region of their formation (at the Antarctic convergence) to the
equator. The substrate of the destruction is the organic matter of the
productive surface Antarctic waters descending in the zone of convergence
(Wyrtki, 1962; Redfield et al . , 1963). This plan is confirmed by data on
the intensification of bacterial destruction at the upper boundary of the
Antarctic waters (see Fig. 17). As we noted earlier, the intensity of the
process of destruction is sufficient to form an oxygen minimum and result
in regeneration of nutrients in 1-3 years.

The concentration of organic phosphorus in the surface topical waters
of the ocean is 0.2-0.4 yg-atom/1 , or 60-80% of the total phosphorus.
Therefore, the processes of local bacterial mineralization of this reserve
of nutrients, consisting primarily of the stable soluble fraction, are of
geat significance in the provision of biogenic nutrition for the
phytoplankton. Ammonia is formed as a result of mineralization of organic
forms of nitrogen by bacteria. In regions where the surface waters are
poor in nutrients, it is consumed by the phytoplankton before it is
oxidized to nitrate. In oligotrophic tropical waters, up to 99% of the
mineral nitrogen is utilized by the phytoplankton in the form of NHt
(Dugdale, Goering, 1967). A portion of the ammonia nitrogen, formea as a
result of mineralization, is oxidized to nitrites and then to nitrates by
the nitrifying bacteria (Watson, 1963; Carlucci, McNally, 1969). It is
presumed that the nitrates of the deep and intermediate waters are formed
due to oxidation of ammonia in the regions of the high-latitude
convergences, where they submerge with the descending waters (Dugdale,
1969).

2.8 Significance of Microbial Biosynthesis in the Cycle of Some
Mineral Elements"

A large-scale biogeochemical process of production of microbial
biomass in the ocean involves carbon plus other elements, which are
included in the composition of the protoplasm of the microorganisms:
nitrogen, phosphorus, iron, trace elements. Data are presented above on
the scale of involvement of inorganic phosphate into the bacterial
synthesis. As concerns nitrogen, the situation should be similar,
particularly with oxidation of organic matter by the microflora in deep
waters and in bottom sediment, but this process is poorly studied. It has
been shown that the marine microflora can cause nitrification and inclusion
of molecular nitrogen into biosynthesis (Maruyama et al . , 1970; Pshenin,
1966). However, it is very difficult to make a distinction between
nitrification of bacteria and of blue-green algae. The total nitrification
in the sea may exceed 300 g/ha«day (Dugdale, Goering, 1964).

Experiments involving the use of the radioisotopes of iron and cobalt
have shown that iron is consumed by bacterioplankton at a rate of 0.5 ug
per mg of organic carbon of the bacterial biomass produced. Cobalt is
consumed by marine bacterioplankton for the synthesis of vitamin 6,0 i" the

276

proportio
are quite
has been
inclusi on
arrives i
hydroxide
the fecal
1972, 197
manganese
consumpti

n of 0.4 pg pe

common in the
established th

in this manne
nto the benthi
s and enters t

matter of the
3a, g). Based

and cobalt by
on of these el

r mg of Cq„„. The bacteria producing this vitamin

sea (SorokTn, 1971a; Lebedeva et al., 1971). It
at the consumption of cobalt by bacteria and its
r in the food chain is the main path by which cobalt
c sediments. This metal does not form insoluble
he bottom sediment in significant quantities with

invertebrates which feed on bacteria (Sorokin,
on analyses of the intensity of consumption of iron,
bacteria and phytopl ankton, the time of total
ements by them has been calculated (Table 10).

Table 10. Calculation of probable time of consumption of the stock of
dissolved iron, manganese and cobalt in the World Ocean by bacteria and
phytoplankton.

Annual assimilation, g

c
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Co

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3.6-]0l3

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1.4-1015

7-10l^

40
40

2.9 The Trophic Role of Microflora in Marine Ecosystems

The concept of the significant role of bacteria in the food chains of
aquatic communities was formulated and a basis provided for it by A. G.
Rodina and S. I. Kuznetsov. They showed, primarily in qualitative
laboratory experiments, that the trophic function of the bacterial
population of bodies of water consists in the conversion of dispersed
organic matter into the matter of microbial cells which are accessible as a
food for invertebrates consuming bacteria. The continuation of
investigations of the structure and functioning of marine ecosystems
(Vinogradov, 1971) required extensive quantitative development of the
problem of the trophic role of bacteria, in order to evaluate the fraction
of microflora in the transformation of organic matter and energy and the
formation of the food resources of marine ecosystems. Studies performed on
board the VITYAZ' and AKADEMIK KURCHATOV in 1968-1974, allowed methodologic
approaches to be developed to the solution of this problem and certain
preliminary data to be obtained.

A quantitative estimate of the significance of microflora in the food
chains of marine ecosystems requires information on the concentrations of
bacterial biomass and the rates of its production, the sources of energy
for bacterial production and the characteristics of effectiveness of
nutrition of massive species of invertebrates by bacteria. The results of
the studies of the feeding of planktonic and benthic invertebrates.

277

performed using ^^C in field conditions as well as in basic laboratories,
showed that natural bacterioplankton can serve as a normal source of
nutrition for infusoria, sponges, hydroids, coral polyps, Appendicularia,
planktonic crustaceans (Cladocera, copepods, euphausiids), bivalves and
gastropods, filtering polychaetes (sabellids, and serpulids), holothurians,
ascidians (Sorokin, 1966, 1971b, 1972, 1973a, d,e; Sorokin et al., 1970;
Pavlova, Sorokin, 1970; Pavlova et al . , 1971; Petipa et al . , 1971, 1974;
Ponomareva et al., 1971). Figure 18 presents the results of determination
of the comparative intensity of nutrition of a number of filter feeders by
phytoplankton and bacterioplankton.

For the fine filter feeders (sponges, Appendicularia, Cladocera,
Polychaeta, veligers, mollusks], bacterioplankton at concentrations close
to the natural ones (0.2-1 g/nr wet biomass) can fully satisfy their
nutrient needs. For many of these species, they are an even more important
source of nutrition than the phytoplankton. The coarse filter feeders
(copepods, euphausiids, bivalve mollusks, ascidians) are unable to filter
out the dispersed bacterial cells and consume primarily the aggregated
portion of the bacterioplankton. They, therefore, use bacterioplankton
less effectively than phytoplankton of the same concentration (Fig. 19).
Nevertheless, for them also, the microbial biomass is an important reserve
of additional food. In experiments involving determination of the
intensity of consumption of labeled bacterioplankton by coarse filter
feeders (Copepoda), with the same concentration of unlabeled phytoplankton

SC

i

'/ I

a

■//

\ Va

Acartia

i

Fig. 18. Daily rations (R, % body weight) of massive spei,ies of plankters
and their nutrition by bacterioplankton (a) and phytoplankton (b). Fine
filter feeders (Oikopleura, Penilia), the veligers (Serpulorbis), medium
filter feeders (Paracalanus) , coarse filter feeders (EucalanusT, and
predators (Acartia). ~~

present, and vice versa (Petipa et al . , 1974), it was shown that the
bacterioplankton represented 30-50% of their diet (Fig. 20). Even such
predacious crustaceans as Euchaeta marina frequently consume
bacterioplankton.

278

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Time, hours

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19. Consumption of natural ^"^C-labeled bacterioplankton containing
aggregates (B) and the same bacterioplankton with aggregates filtered
by a membrane filter (A) by a fine filter feeder--the sponge Toxadocea
(1) and a coarse filter feeder-- the oyster Crassostrea gigas
radioactivity of labeled bacteria in water, 10-^ desintegrations
ml .

R =
per minute/20

Using the ^^C-labeled bacterioplankton, the optimal concentrations of
bacterioplankton for the nutrition of coarse and fine filter feeders were
determined (Fig. 21). For the coarse filter feeders, the optimal
concentration of bacterioplankton is that at which the bend occurs in the
corresponding curves, at 1-1.5 g/m"^. These values are characteristic for
littoral eutrophic marine biotopes or the layers of maximum concentration
of plankton in highly productive upwelling zones (see Table 5). In these
waters, even coarse filter feeders can supply their nutritional needs by
eating bacterioplankton. For fine filter feeders, the optimum
concentration is 0.2-0.4 g/m-^. These concentrations are found in the
layers of maximum concentration in boreal waters in the summer, the neritic
waters of boreal and tropical areas, and the pelagic zone near the tropical
divergences. Thus, over a significant portion of the ocean, fine filter
feeders can fully satisfy their nutritional needs by means of
bacterioplankton alone.

The bacteria are as
assimilation of phytopla
Pavlova, Sorokin, 1970;
daily rations of fine fi
veligers, Appendicularia
bacterioplankton amount
expenditures of these an
weight. Therefore these
expenditures by feeding
less than the optimal (P
Sea cladoceran Penilia a
which the crustacean can
only 50 mg/m-^, significa
the littoral zone.

similated to 40-60%, close to the level of

nkton (Sorokin, 1968; Sorokin et al . , 1970;

Pavlova et al . , 1971; Petipa et al . , 1974). The

Iter feeders with small body size, such as the

, Cladocera, hydroids when feeding on

"to 50-100% of their body weight. The daily

imals for metabolism amount to 15-20% of their body

animals can compensate for the metabolic
with bacteria at their concentration 3 to 5 times
avlova, Sorokin, 1970). For example, for the Black
virostris, the threshold concentration of food at

compensate for its metabolic loss was found to be
ntly lower than the biomass of bacterioplankton in

Special studies of the role of bacterial nutrition have been
undertaken for bottom filter feeders of the tropical shelf. These

279

!{I0

SO

•i/\

ka.

J

ISJo/o

■.b '■:•

5

Fig. 20. Importance of various food sources in the formation of the diet
of some common species of mesoplankton in the area of the equatorial
divergence in the Pacific Ocean: R - daily ration (% of body weight); b -
bacterioplankton; P - phytoplankton; Ci - ciliates; a - animal food
(mixture of small calanoids); 1 - Clausocalanus sp.; 2 - Paracalanus
parvus; 3 - Undinula darwini ; 4 - Eucalanus attenuatus; 5 - Acartia clausi ;
(Petipa et al . , 1975).

Biomrss of bacteria, mg/m^
/^"S 27i; SS<?

-"■f OJ f.2 /.5 /,s

Total number of bacteria (lO^/m.?.)

Fig. 21. Variation of intensity of nutrition (R, %) of some mass species
of marine invertebrates with bacterioplankton as a function of its
concentration: 1 - the sponge Toxadocea; 2 - the veligers Vermetidae; 3 •
the polychaete Megalomma; 4 - the coral Pocillopora; 5 - the oyster
Crassostrea; 6 - the copepoda Eucalanus.

280

experiments showed that oysters, polychaetes, sponges and ascidians are
capable of normal feeding on bacterioplankton at its natural
concentration. Their nutrition in this case is no less than it would be if
they fed on fine phytoplankton. The filtering rate was 200-600 1/g of
organic carbon in the body of the animals per day. It was found that coral
polyps can also consume bacterioplankton (Sorokin, 1972, 1973a, b, e). The
capability of coral to digest the bacteria they consume was proven by
measuring the radioactivity of CO2 liberated by them after feeding on
labeled bacteria.

One important intermediate trophic link allowing the utilization of
bacterioplankton in the food chain are the Protozoa: the ciliates
(Tintinnidae, Strombidium) and the colorles flagellates such as Bodo
(Fenchel, 1970; Fenchel , Reidl, 1970; Johannes, 1965; Petipa et al . ,
1974). The protozoans consume bacteria and themselves serve as food for
the crustacean micro- and mesozooplankton (Mordukhay-Boltovskaya, Sorokin,
1965; Monakov, Sorokin, 1971; Pavel 'yeva, Sorokin, 1971). In the boreal
sea basins, the Protozoa develop in mass after the decay of phytoplankton
at the end of the spring bloom which cause an increase of the biomass of
bacteria. The biomass of ciliates and colorless flagellates may reach
1 g/m^ in the open sea in the layer of the main maximum up the thermocline,
exceeding the biomass of the remaining zooplankton. Massive development of
bacteria and Protozoa represents an important stage in the heterotrophic
phase of the seasonal succession of the plankton community in the temperate
waters. During this period, they are actively consumed by calanoids
(Sorokin, 1974). The Protozoa are one of the leading components in the
plankton community of the regions of upwellings (Beers, Stewart, 1971;
Tumantseva, Sorokin, 1975).

As was noted above, bacteria and Protozoa represent the main
nutritional component of detritus and of the bottom sediments. Direct
microscopic observations (Newell, 1965; Fenchel, 1972) have shown that in
the detritus which passes through the intestines of benthic animals, the
population of bacteria is decreased several times due to digestion (Newell,
1965; Johannes, Satomi, 1966). Experiments with ^T have proven the
digestion of bacteria by amphipod sestonophages (Hargrave, 1971).
Holothurians and gastropods digested the labeled microflora in the bottom
sediments available to them, which provided them with a normal ration
(Sorokin, 1972).

Direct correlation in the distribution of the biomass of bacteria and
meiobenthos in the oceanic benthic sediment (Table 11) indicates that the
bacteria represent the main nutritional component of the meiobenthos.
Actually, the microflora in the sediment forms the predominant portion of
the living available protein. In deep-water sediments of the oligotrophic
areas of the oceans where the concentration of microflora is very low there
are no benthic animals which nonselectively swallow the bottom (Sokolova,
1972).

An overall evaluation of the trophic significance of the microflora
can be produced only at the level of the ecosvstem by calculating the
fraction of its participation in the transformation of matter and energy of
the entire community. In order to produce the corresponding information,
microbiologic analyses should be conducted in combination with

281

determination Table 11. Mean values of biomass of bacteria and meiobenthos
(g/nr, wet mass) bottom sediments of various trophic zones of the Pacific
Ocean (Sorokin, 1970d; Sokolova, 1972).

Type of Sediment Bacteria Meiobenthos

Detrital sediments of littoral zone
Sediments of eutrophic shelf
Sediments of mesotrophic slope
Deep-water sediments of oligotrophic zone

100 -500

20 -50

20 -100

10 -30

2 - 20

1 -10

0.2- 2

0.05- 1

of the production and biomass of the main components of the community.
Work of this sort was performed during biologic voyages of the VITAYAZ' and
AKADEMIK KURCHATOV (Vinogradov, 1971). An example of one of the diagrams
of flows of energy in ecosystems of the pelagic zone is shown in Fig. 22.
The diagram characterizes the participation of microflora in the
transformation of energy in the ecosystem of the pelagic zone of the Sea of
Japan in the summer (Sorokin, 1974). In the summer, after the heating of
the water and formation of the thermocline, nutrients in the upper, mixed
layer, 20-30 m thick, are rapidly consumed by phytoplankton, the main
portion of which dies, and only a small fraction is retained, vegetating at
the upper boundary of the thermocline in the layer of the primary maximum
at a depth of 25-35 m. Most of the biomass of plankters consists during
this period of heterotrophic bacteria and Protozoa, which represent about
2/3 of the metabolism and energy flow in the ecosystem. The energy of
primary production here satisfied only 40% of the energy requirements of
the heterotrophs. The remaining energy arrives from the stored energy of
organic matter, created during the winter and spring bloom of the
phytoplankton, which occurs during a period of low temperatures, when the
metabolism of the heterotrophic forms is low. The energy of this organic
matter is expended during the heterotrophic phase of the seasonal
succession of the plankton community. About 70% of the respiration of all
the plankton community is accounted for by bacterioplankton, about 15% by
Protozoa: the ciliates, tintinnids, and colorless flagellates, which
develop massively during this period in the layer of the main maximum and
represent the primary food base of the copepods.

Thus, the basic trophic function of the microflora of the temperate
waters consists in the transformation of the excess organic matter
accumulated during the period of the bloom into microbial biomass, which,
directly or via the Protozoa, as an intermediate linkage serves as an
additional food source for the zooplankton during the summer period of low
phytoplankton production.

In the productive region of the equatorial divergence, the bacterial
population represents 70% of the metabolism of the heterotrophic portion of
the community (see Table 4). The heterotrophic community is incapable of
consuming and converting the mass of primary production created. The
excess organic matter is carried by flows in the form of detritus and
dissolved organic matter into the poorer regions of the ocean, where it is

282

Phytopl.inkton
r - 4/:o

Rcsor^-r:

"■f ornanlc

irutccr accur^uiatcH [

during t

•<•■ bprlns

bloom ol

,''■'■, -opljnk-

ton COO

O')0)

TS^

Sediacnc^clon Co
Bottoia

Fig. 22. Diagram of flows of energy (cal/m^ per day) in pelagic community
of central portion of Sea of Japan in the summer. Symbols same as in Fig.
12.

included in the production process by bacterioplankton and Protozoa. In
the oligotrophic tropic waters and even relatively productive waters of the
equatorial divergence, the primary production is insufficient to cover the
energy cost of the heterotrophic portion of the community. This cost is
covered by including into the metabolism, via the bacterial activity, the
reserves of dissolved and suspended organic matter carried in by currents
from the upwel lings and subpolar convergences, where an excess of organic
material is created, which is not processed by the local heterotrophic
community. In the oligotrophic waters, 80-90% of the flow of energy and
metabolism of the heterotrophic portion of the community is accounted for
by bacteria and Protozoa, only 10-20%--by the remaining micro- and
mesozooplankton. The same conclusion is reached as a result of direct
measurements of the relationship of intensity of respiration of meso- and
microplankton in tropical waters of the Atlantic (Pomeroy, Johannes, 1968).

To calculate the energetics of an ecosystem, the metabolism of which
include external organic matter carried in from other regions of the ocean,
it is very important to determine the size of this external "input". This
can be done by comparing the actual production of bacteria with that which
can be created by using the "internal" primary production (Sorokin,
1973d). The total energy input of the ecosystem (PP) consists of the
energy of the "internal" primary production (?„) and the energy of the
external organic matter included in the production process through the
bacterial link. The value of PP can be calculated if we know the primary

283

production (?„) and the summary production of bacteria (P\^) , using the
equation: PP = Pk + 0.84 Pp. Examples of calculation are presented in
Table 12. The calculations show that in tropical waters, the production of
primary food may be several times more than the production of
phytoplankton.

The calculations presented above demonstrate the important role of
bacteria in providing a spatial energy connection between biotopes with
different levels of productivity: upwellings and oligotrophic waters,
subantarctic and tropical waters. In temperate waters, the microflora
provide the energy connection between phases of the seasonal succession of
communities. In littoral and benthic biotopes, it transforms the energy of
the mass of dead organic material of the benthic sediments and detritus,
dissolved organic matter, and reduced mineral products of anaerobic
decomposition into living organic matter of the microbial biomass which can
be assimilated. It thus forms the basic food resource, utilizing various
local and external sources of energy.

Based on the information concerning the trophic structure of marine
ecosystems, data on the magnitudes of rations, production of bacteria and
other heterotrophic microplankton, an attempt was made to compose an
approximate diagram of the flows of energy in the ecosystem of the World
Ocean (Fig. 12) and, on the basis of the energy consumption of
heterotrophs, to estimate the probable necessary "input" of energy into the
ecosystem--primary production. Data on the production of benthos and
zooplankton were taken from the works of Bogorov (1968, 1974). The biomass
of microzooplankton was calculated considering data on the relationship of
biomass of meso- and microzooplankton (Beers, Stewart, 1971; Tumantseva,
Sorokin, 1975). The approximate production of nekton was calculated on the
assumption that the total production of fish is 30 times greater than the
total catch.

We find that some 80% of the energy of primary production is utilized
through the detrital food chain, with the participation of bacteria and
microzooplankton. This conclusion is in agreement with the data indicating
a significant predominance of dead organic matter in any marine biotope.
Even in the euphotic zone, the total carbon of plankton, including
bacteria, is only 3-lOX of the suspended organic carbon and about 0.5% of
the total organic carbon in sea water (Finenko, Zaika, 1970). The direct
grazing of phytoplankton by animals is about 25%, which agrees with the
data on the consumption of phytoplankton in the North Atlantic (Riley,
1957). The respiration of meso- and macrozooplankton represents about 15%
of the total respiration of heterotrophs, the remaining portion being
accounted for by microplankton (bacteria and microzooplankton), which
agrees with the results of direct determinations (Pomeroy, Johannes, 1968).

Although the ration of animals was assumed minimal, the trophic
relationships in the ecosystem are found to be quite highly stressed, even
if the input of primary energy is assumed to be 7.6 -lO^' kcal , or about
8*10^^ t of carbon per year, which is 3.5 times greater than the primary
production calculated by means of the radiocarbon method (Koblentz-Mishke
et al., 1968). It is quite probable that future direct determination of
this value, based on recalculated and improved radiocarbon methods will
yield the same quantity: (7-9) '10^^ t C per year (Eppley, 1981).

284

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285

3. Production of Zooplankton. (E. A. Shushkina)

Determinations of the rate of production of planktonic organisms
makes it possible to estimate the production of animals at various
trophic levels and the plankton community as a whole, and to approach a
determination of the regularities of functioning of pelagic ecosystems.

Beginning early in the 20th century, studies of the production of
aquatic animals and their communities were developed throughout the
prewar years (Zenkevitch, 1931; Brotskaya, Zenkevitch, 1936; Winberg,
1936; Yashnov, 1940; Juday, 1940; and others). As a result of the study
of the biologic specifics of aquatic organisms of various trophic
levels, approximate estimates were produced of the specific rates of
their production (P/B coefficients).

In the postwar years, interest in the problem of biological
productivity in aquatic environments increased still further, leading to
the accumulation of extensive factual material on the production
primarily of phyto- and bacterioplankton (Winberg, 1960; Strickland,
1960, 1971; Steemann Nielsen, 1960; Koblentz-Mishke et al . , 1970;
Sorokin, 1973e, g; and others). The studies of production of organisms
of upper trophic levels (zooplankton zoobenthos, fish) developed more
slowly (Zenkevitch, 1947; Greze, 1951; Elster, 1954; Shcherbakov, 1956;
Kamshilov, 1958, etc.). However, since the 1960's, the problem of
effective utilization of biologic resources of bodies of water became
more acute, leading to a rapid increase in the number of works on
estimation of the rate of production of aquatic animals, both at the
populations level (Mednikov, 1960; Konstantinova, 1961; Stross et al . ,
1961; Greze, Baldina, 1964; Mull in. Brooks, 1970; Malovitskaya, 1971;
Greze et al . , 1971; Shushkina et al . , 1974), and for entire trophic
levels of zooplankton (Edmondson et al., 1962; Pechen', Shushkina, 1964;
Zaika, 1969; Mull in, 1969, Greze, 1970; Petipa et al . , 1970; V. D.
Fedorov et al., 1975). These materials, produced by more precise
methods than those used in the earlier years, based on a combination of
experimental and field studies, allow us to approach the estimation of
the intensity of the production of aquatic communities as an assemblage
of organisms at various trophic levels.

In recent years, the number of studies of the production process at
the community level has rapidly increased (Raymont, 1966; Petipa, 1967a;
Petipa et al . , 1970; Parsons et al . , 1969; Winberg, 1973; Vinogradov et
al., 1973). One basic method used to perform the most important task of
modern hydrobiology--that of studying the regularities of functioning of
aquatic communities, predicting and, in the final analysis, controlling
their biologic productivity--is mathematical simulation of processes
defining the function of aquatic ecosystems. This method has been ever
more widely used in the past decade in the study of various problems
related to the growth and production of aquatic organisms (Bekman,

286

Menshutkin, 1964; Menshutkin, Prikhod'ko, 1968; Brocksen et al . , 1970;
Zaika, 1973; Shushkina, Kislyakov, 1975), the productivity of ecosystems
(Menshutkin, 1967, 1971; Smith, 1972; Gupta, Houdeshell , 1973; Steele,
1974; V. I. Balyayev, et al . , 1974; Winberg, Anisimov, 1969; Vinogradov
et al . , 1971, 1975, 1976). The significance of mathematical modelling
for the solution of the problem of effective utilization of the natural
resources of bodies of water is quite obvious (Krogius et al . , 1969;
Menshutkin, 1971; 1972; McKenzie, Mathisen, 1971).

In spite of the successes achieved in the study of the rate of
production at various levels of organization of aquatic communities
(species population, trophic level, community as a whole), the available
data are insufficient to reveal the general regularities which define
the level of production of animals in various regions of the ocean and
in various geographic zones. However, in recent years some summarizing
works along this line have appeared for both marine and fresh-water
ecosystems (Raymont, 1966; Winberg, 1968; Mullin, 1969; Mann, 1969;
Greze, 1971, 1973a, b; Zaika, 1972; Gushing, 1975; Winberg et al . , 1974;
Bougis, 1974; Steele, 1974).

Unfortunately, the production estimates of various authors were
made by diverse methods, with various degrees of accuracy, for various
seasons and periods of time, which makes any attempt to summarize the
available materials and come to any definite conclusions concerning the
level of production of aquatic animals in different geographic zones
still more difficult. Nevertheless, it is clear (Greze, 1973a) that in
the boreal regions of the ocean (Bering and Barents Seas, Northern
Pacific) the annual secondary production is lower than in the southern
regions (Black and Azov Seas, tropical Atlantic). The same patterns are
apparently true for fresh-water ecosystems (Winberg et al . , 1974;
Winberg, 1975). It seems desirable to attempt to summarize the
materials accumulated to date on the rate of production at various
levels in pelagic communities in waters of varying trophic levels in the
most studied tropical regions of the ocean and the southern seas of the
USSR.

The factual material presented below was obtained primarily during
expeditions conducted by the Institute of Oceanography, Academy of
Sciences, USSR and, in order to avoid repetition, is only compared with
results obtained and discussed in review publications of recent years
(Greze, 1970, 1971, 1973a, b; Bougis, 1974; Steele, 1974; and others).

It must be emphasized that with all methods of estimation of the
production rate for all trophic levels of a planktonic community,
complete study of the ecosystem is necessary; it is particularly
important that information be available on the concentrations of all
elements of plankton in a single sample. This allows us to avoid or at
least minimize the bias of estimates resulting from nonuniformity of
distribution of elements of the community, unavoidable when different
types of equipment are used to catch specimens at different times. In
recent years, in the expeditions of the Institute of Oceanography, high
capacity water bottles (100-150 a) have been used, allowing us to
determine the concentration of practically all plankton elements with

287

the exception of large mobile macrozooplankton, in a single water sample
{Vinogradov et al . , 1976)

3.1
Ecolog

Methods of Calculation of the Secondary Production and
)gic-Physio1ogica1 Characteristics of Planktonic Animals

The methods of determination of the production of aquatic animals
are outlined in a manuscript edited by G. G. Winberg (1968) and refined
and supplemented in later works (Zaika, 1972; Greze, 1973a, b; Bougis,
1974).

Since we will be discussing basically the productivity of
zooplankton in tropical regions of the ocean, where the doubling time of
animals is long, it makes sense to discuss briefly the obstacles and
specific features of determination of the production rate in populations
which are constantly supplemented. In estimating the production of
populations of this type, the most precise values are yielded by the
graphic method used by G. G. Winberg and V. N. Greze, which is widely
used in production studies in sea and fresh water. To determine
production by this method, we must know the doubling rate of the
animals, the time of development of individual age stages and the age
composition of the population at known time intervals. Whereas it is
rather easy to produce this information for the populations of fresh
water, for marine areas, particularly open regions of the ocean with
complex hydrologic conditions and significant nonuniformity of the
distribution of plankton, both vertical and horizontal reliable material
on the age composition of the population is exceedingly difficult to
obtain, to say nothing of the difficulties involved in the study of the
times of development of animals in multispecies communities. Although
large numbers of publications have appeared in recent years, reporting
successful cultivation and study of the time of development of
individual species of zooplankton (Sazhina, 1968, 1974; Mullin, Brooks,
1970; and others), the question arises of the correctness of simple
transfer of data obtained in the laboratory to natural populations.
Therefore, as yet the use of the graphic method for determination of the
production of populations and communities in the pelagic zone of the
ocean is difficult although, for example, this method has been
successfully used for the Black Sea (Greze, Baldina, 1964; Greze et al . ,
1968; 1971, 1973; G. N. Mironov, 1970, 1973; Petipa et al., 1970).

The physiologic method is more applicable for estimation of the
rate of production in tropical planktonic communities (Winberg, 1964,
1968). To determine production by this method, we must know the number
of animals N, their weight W, the mean daily metabolic rate R and
coefficient of assimilated food used for growth Ko. Then, the mean
daily production of the population P can be calculated from the equation

r-n^

NW (3.1)

Calculation of the production by graphic and physiologic methods
yields similar results (Shushkina, 1972).

288

In estimating the production rate, all characteristics related to
production, weight and metabolism are expressed in common units of
measurement, preferably in units of energy--calories. This brings up
the need to determine the energy equivalents of body mass and calorie
content of the basic elements of the planktonic community. The
energetic approach to the study of communities permits one to ignore, to
a certain extent, their species composition, but in return it is very
exacting in regard to information on their trophic and spatial
structure.

The results of determination of the energy equivalents of body mass
Wg (cal/indiv.) as a function of length % (mm) for abundant planktonic
animals in the tropical Pacific (Shushkina, Sokolova, 1972), which can
be used for production estimates, are shown in Figure 23. Using these
regressions Wq[i) and knowing the mean length of animals of a given
taxon, we can determine the mean body weight in calories Wg.

It is usually thought that planktonic animals in the higher
latitudes, due to their higher content of fat, also have a higher
caloric equivalent. However, comparison of the caloric equivalent of
mysids in the tropical regions of the Pacific, the Black Sea and the Sea
of Japan, (Fig. 24a) and chaetognaths in the same tropical regions, the
North Atlantic and Sea of Japan (Fig. 24b) showed no significant
difference, although it is quite probable that for other species of
zooplankton, i.e., copepoda, the differences in calorie content would be
greater.

The regression Wg(£) for tropical animals of various taxonomic
groups is used to calculate the mean caloric equivalent (Kcal/mg wet
mass). The wet mass of animals of the groups studied was usually
determined by weighing, or from the dimensions of the body, using
nomograms, or empirical equations. The mean caloric equivalents thus
calculated for tropical phytoplankton, zooplankton, and bacteria
(Sushchenya, 1969; Troitskiy, Sorokin, 1967; Sorokin, 1971) are
presented in Table 13.

Rate (R) and intensity (R/W) of metabolism of planktonic animals,
usually determined on the basis of the rate of consumption of oxygen,
are necessary for an estimation of the rate of production of
zooplankton, the flow of energy through a planktonic community and the
succession characteristics of pelagic ecosystems.

Measurement of metabolic rates in marine and fresh-water animals
has been the subject of a large number of reports (reviews: Sushchenya,
1969, 1972). For marine zooplankton of various regions of the ocean,
rather extensive material has been obtained by the expeditions of the
Institute of Oceanology (Shushkina, Vilenkin, 1971; Shushkina, 1972;
Kukina, Chistov, 1972; Shushkina, Pavlova, 1973; Pavlova, 1973;
Kuz'micheva, Kukina, 1974; Klyashtorin, Kuz'micheva, 1975; Klekovskiy et
al., 1975; Pasternak, 1976; Musaeva, Vitek, 1975). It has been
suggested that the values of metabolic rates obtained in these
experiments are significantly low due to the limited movement of the
animals in the closed experimental bottle (Gruzov, 1972; Pavlova, 1973,

289

Table 13. Caloric equivalents (Kcal/mg wet weight) of the component
plankton corrnunities of the tropical Pacific.

Group of organisms Dimensions, mm

Phytoplankton (small and large)

0.6

Bacteria (dispersed and aggregated)

---

1.0

Flagellata and Infusoria

—

0.8

Calanoida "broad" (length:width = 3:

1)

0.5

- 10

0.75

Calanoida "narrow" (length:width = 4

:1)

2

- 6

0.4

Cyclopoida (Oncaea, Corycaeus)

1

- 2

0.7

Oncaea venusta, females with eggs

1

- 3

1.0

Euchaeta marina, females with eggs

2.5

- 3.5

1.5

Euphausids

2

- 10

0.8

Ostracoda

0.8

- 3.0

0.7

Hyperiidae

2

- 3

0.7

Appendicularia

7

- 10

0.06

Salpae

7

- 10

0.01

Medusae

3

- 8

0.03

Ctenophora

2

- 10

0.03

Siphonophorae

3

- 10

0.005

Chaetognatha such as Sagitta bipunctata

3

- 10

0.9

Chaetognatha such as S. enflata

10

- 40

0.4

Pteropoda

0.6

- 5.0

0.35

Polychaeta "narrow" (length: diameter

=

6-10:1)

6

- 10

0.6

Polychaeta "broad" (length: diameter

=

3-4:1)

3

- 5

0.8

1974); however, studies of recent years (Kuz'micheva, Kukina, 1974;
Klyashtorin, Kuz'micheva, 1975; Musaeva, Vitek, 1975) have indicated
that the values of rate of oxygen consumption obtained in closed
bottles, are only slightly lower and are quite suitable for approximate
estimates of production using the physiologic method. As concerns the
influence of feeding conditions on this parameter, individual
observations have shown that the metabolic rate does not actually depend
on the concentration of food (Shushkina, 1966; Shushkina, Klekovskiy,
1968; Kryuchkova, 1972).

Some results of measurement of metabolic rate R as a function of
body weight Wg, cal , for planktonic animals in the tropical water of the
Pacific Ocean are presented in Figure 25. A comparison of the values of
metabolism for copepoda in the oligotrophic regions of the Pacific at
30°C (Shushkina, Pavlova, 1973) with metabolism measured in the regions
of the equatorial upwelling at 20-22°C (Musaeva, Vitek, 1975) showed
that there was no significant difference (Fig. 26). If the regression
line of metabolism R to weight W at 30°C is adjusted to 20°C, using the
temperature correction suggested by L. M. Shushchenya (1969), the

290

Log W

/,/

^is

a.'f

-.acf

■A8

-f.2

log rt'^

i^.S

^«

-P,f

-OJ

-f.l

/

/

'-J.Z 0 O.l C^ t7,d- D.d 1.0 /.I io<l^, mrp

Fig. 23. Caloric equivalents of body mass Wg (cal/indiv.) of tropical

planktonic animals of various lengths I (mm), a - crustaceans: 1 - Calanoida,

length:width = 3-3.5:1; 2 - Calanoida, length:width = 2-2.5:1; 3 - Eucalanus

attenuatus; 4 - Euphausiacea; 5 - Mysidacea; 6 - Lucifer; 7 - Hyper i idea;

8 - Ostracoda; b - other; 1 - Chaetognatha; 2 - Medusae; 3 - Ctenophora;

4 - Siphonophora; 5 - Salpae; 6 - Appendicuiaria; 7 - Polychaeta; 8 - Pteropoda.

291

/.a

0.S

0.Z
0

-0,1

-p,e
-',c

a

I y

■I
J

-/,*

' 0,3 ff.¥ 0,5 0,6 0,7 {J,S ff,0 /,0 /,! /, Z /.Jloql*""

Fig. 24. Caloric equivalents of body mass Wg (cal/indiv. ) as a function of

size (mm) of mysids (a) and chaetognaths (b) of various latitudes.

a - 1 tropical waters (reported by E. A. Shushkina and I. A. Sokolova);

2 - Sea of Japan (reported by E. A. Shushkina and V. I. Kuz'micheva) ; 3 - Black

Sea (reported by V. N. Mikheyev); b - 1 - tropical waters (reported by E. A.

Shushkina and I. A. Sokolova); 2 - Sea of Japan, littoral waters (reported by E. A.

Shushkina and A. G. Timonin); 3 - Sea of Japan, open sea (reported by I. V. Kukina);

4 - Antarctic waters.

292

^.0

ro
(J

E

P.6

h-
o

IS

— 1

l"/

Z2

/,s

f.'*

f.o

D.S

'/J 2,0 2,Z l.U- 2,6 2,8 3,0 3,2 3^ 3,f 3.8 U,0 f.Z U,U

Log We> mcal/indiv.

Fig. 25. Dependence of the rate of respiration R (meal /day per
individual) upon the body weight Wg (mcal/indiv.) in tropical planktonic
animals, a - crustaceans: 1 - Calanoida; 2 - Cyclopoida; 3 -
Euphausiacea; 4 - Mysidacea; 5 - Ostracoda; 6 - Hyperiidea; 7 -
Lucifer: b - other: 1 - Chaetognatha; 2 - Medusae; 3 - Ctenophora; 4 -
Siphonophora; 5 - Polychaeta; 6 - Pteropoda.

regression line presented falls significantly below the line obtained
experimentally at 20°C. Thus, we can draw the preliminary conclusion
that the level of metabolism of tropical copepoda at 30°C is close to
the level of metabolism of crustaceans of the temperate latitudes at
20°C. This confirms once more the opinion that the metabolism of
animals at different latitudes is adapted to the environmental
temperature (Fox, 1936; Sholander et al., 1953; Pavlova, 1967;

293

Sushchenya, 1969, 1972; Shushkina, Vilenkin, 1971; Edwards, 1973). In
calculating the production of tropical zooplankton in the euphotic layer
from the metabolic rate, the temperature corrections apparently should
not be introduced.

Calculation of the mean daily value of production by the
physiologic method presumes knowledge of the mean coefficient of
utilization of assimilated food for growth K2 for the population or
group of animals studied. As follows from equation (3.1), the value of

r,8 Z,g 2,2. 2.'^ 2.S 2,8 3,0 3,2 3^ 38

Log Wg, mcal/indiv.

Fig. 26. Dependence of the metabolic rates R (meal/day per individual)
upon the body weight W (mcal/indiv.) for copepoda at various t, C. 1 •
tropical Calanoida at 30°C (Shushkina, Pavlova, 1972); la - same,
adjusted to 20°C using temperature correction suggested by L. M.
sushchenya (1969); 2 - tropical Calanoida at 20°C (Musaeva, Vitek,
1975); 3 - Calanoida at 20°C (Sushchenya, 1969).

K2 is determined by the ratio of production to assimilated food, i.e.,
to the sum of production plus the cost of metabolism. Determination of
production requires regular observation of the growth of animals, plus
knowledge of the regularities and rates of their breeding. Therefore,
the volumes of accumulated factual material on the values of K2 for
aquatic animals is not sufficient to allow reliable conclusions to be
drawn, although a number of works have been published, dedicated to the
analysis of the variability of this coefficient (Sushchenya, 1969;
Shushkina, Klekovskiy, 1966; Kryuchkova, 1967, Sushchenya, 1970; Ivlewa,
1970; Mullin, Brooks, 1970; Soldatova, 1970; Shushkina, 1972; Bougis,
1974; Zaika, 1974; Pasternak, 1974; Khmeleva, 1967). The studies which
have been performed indicate several conclusions concerning probable
changes in maximum and average values of K2 and the influence of
environmental factors on this quantity.

For rapidly growing species and populations under optimal
conditions, the value of K2 is near 0.6 (Winberg, 1964, 1973; Klekowski,
Shushkina, 1966; Sushchenya, 1970), although during some periods of
development (embryonal, older nauplial stages of copepoda, young
cladocera, etc.), K2 may be as high as 0.7-0.8 (Winberg, 1956, 1968;
Zaika, 1974; Bougis, 1974). Many authors assume that for natural
populations of aquatic animals, the mean value of '^o is closer to 0.3-
0.4 (Winberg, 1966; 1973; Sushchenya, 1970; Greze, 1971; Shushkina,

294

1972; Pasternak, 1974, Zaika, 1974).

It is probable that the value of Kp depends directly on temperature
(Ivlewa, 1970; Mull in, Brooks, 1970) and feeding conditions (Klekowski
et al., 1972; Winberg, 1968; Klekovskiy, Shushkina, 1968; Mullin,
Brooks, 1970) and changes irregularly with the age of the animals
(Dryuchkova, 1967; Soldatova, 1970; Shushkina, 1972; Klekovskiy,
Shushkina, 1977), particularly if the value of production defined
considers the increase due to formation of reproductive products and
exuvia (Kmeleva, 1967). On the other hand, many authors report sharp,
irregular fluctuations in the values of K2 in various stages of
development of aquatic animals (Soldatova, 1970; A. F. Pasternak, 1974).

Studies have shown that in calculating the mean daily value of
production of zooplankton on the basis of the physiologic method, one
can take K2 = 0.3-0.4 as the average value for a specific population,
with 0.6 as the maximum value.

An estimate of the rate of production of individual trophic levels
(specific associations) in the communities studied can be obtained by
adding the production of specific populations of animals of the trophic
level in question, if there is no cannibalism. In certain cases, the
rate of production of phytophagous planktonic animals can be estimated
by the radiocarbon method (Chmyr, 1967); however, methodologic
difficulties make it necessary to correct the results produced by other
methods (Shushkina, Sorokin, 1969). Individual comparison of the values
of production determined by the radiocarbon and physiologic methods have
yielded similar results (Shushkina, 1971; Malovitskaya, 1971).

3.2 Methods of Calculation of the Production of Communities

Production rates of communities consisting of organisms of various
trophic levels cannot be determined by simple addition of the production
of individual trophic levels, since this sort of addition yields a
clearly elevated estimate.

Net production of the whole plankton community (Pq). which
according to Winberg (1960) is equal to:

Pq = Pp -.L Ri (3.2)

^ i=B

where Pp is primary production, R^- is the metabolic rate of different
elements of the community from bacteria (b) to predatory animals (s).

The value Pq can also be calculated in another way (Zaika, 1972;
Shushkina, 1966):

s s s s s

Po =.l Pi +.LDi -.yCi =,l Pi -.y Ci-Uj^ (3.3)

i=p 1=8 i=B l=p 1=8

295

where P^- is production of different elements of the community from
phytoplankton (p) to carnivores (s), D^ - nonassimilated food; C^- -
value of food consumption; U"-'- - food assimilability .

Both equations (3.2 and 3.3) are practically the same.

It is possible to calculate the part of community production that
may be utilized by higher trophic levels not accounted for in the
calculations (carnivorous fishes, squids), or by any other form of
exploitation (Shushkina, 1966; Klekowski, 1970).

It is real community production (P^,):

P2 =.l Pi -.LCi (3.4)

i=a i=f

where P^ is production of different elements of community from
protozoans (a) to predatory animals (s) and C^- is value of food
consumption of the elements from herbivorous animals to predators.

The rate of production of a planktonic community can be calculated
using equation (3.4) if the community includes only a small number of
species, interrelated primarily by the trophic chain. Communities of
this sort are relatively frequently seen in fresh and marine bodies of
water in the temperate and high latitudes. However, in this case as
well, the calculation of the production of zooplankton is rather
difficult, since it requires us to consider the influence of such
environmental factors as temperature, concentration of food for each
element of the community, etc., on all of the parameters included in
equation (3.4). Calculations of production for an entire tropic pelagic
community, consisting of hundreds of species, interconnected in a
trophic chain, are practically impossible without the use of
mathematical modelling and computers.

The method of mathematical modelling in combination with
radiocarbon and physiologic methods, can be used to estimate the rate of
production of individual specific populations (Shushkina et al . , 1974),
the trophic levels of zooplankton and the planktonic community as a
whole (Shushkina, Kislyakov, 1975). Such a combination of different
methods was, for example, used to estimate the productivity of pelagic
communities of the Sea of Japan (52nd cruise of the VITYAZ) and the
equatorial zone of the Pacific Ocean (17th cruise of the AKADEMIK
KURCHATOV). The essence of the approach is that at the level of maximum
concentration of plankton, large (140 i) water bottles of organic glass
collect samples of water, including a known quantity of phytoplankton,
preliminarily labeled with radiocarbon to a constant level. After 10 or
12 hours exposure of the water bottle at the same depth during the dark
hours of the day, the concentration N, dimensions i, weight W and
radioactivity G of organisms of the phytoplankton, bacteria, protozoa
and individual systematic or trophic groups of zooplankton (fine filter
feeders, small herbivores, cyclopoids, predaceous calanoids, etc.) are
determined. A plan is then constructed of the basic trophic connections

296

between the elements of the community which are distinguished,
nutritional selectivity coefficients are selected and the increase in
weight (production) per unit of time (per day) is described for each of
the elements distinguished:

dWi _i

-^= CiUi' - Ri (3.5)

It is desirable to consider how the assimilation Uj is influenced
by the degree of trophicity of the waters, membership in a predaceous or
peaceful level of zooplankton, as well as the variation in the daily
diet Cj as a function of concentration of food (Ivlev, 1955; Jergensen,
1955; Petipa, 1967; Winberg Anisimov, 1969; Petipa et al . , 1971). The
assimilation of the food U"^ = (P + R)/C, apparently depends to some
extent on the trophicity of the water, i.e., on the concentration of
food, and decreases with increasing food concentration (Jergensen, 1955;
Klekowski et al . , 1966; Petipa et al . , 1971, 1974). It is thought that
the minimum value of assimilation U"j , with an abundance of food, is
near 0.4 (Winberg et al., 1965; Klelciwski, Shushkina, 1966; Klekowski,
et al . , 1972; Petipa et al . , 1975). For carnivorous animals, the
assimilation of food is usually higher than for herbivorous animals
(Soldatova et al . , 1969; Monakov, Sorokin, 1972; Winberg, 1973). The
mean value of assimilation for herbivores can be assumed to be close to
0.6 (Conover, 1966; Sushchenya, 1975), for predators--0. 7-0.8.

The rate of metabolism R^- is determined experimentally by the
method of Winkler or by a polarographic method for animals of each
element in the community (Shushkina, Pavlova, 1973; Muscaeva, Vitek,
1975; Klekovskiy et al . , 1975). All of the ecologic-physical indices
included in equation (3.5) are expressed in calories.

It is assumed that the radiocarbon label introduced with the
labeled phytoplankton to the portion of the planktonic community
isolated in the water bottle is distributed among the elements of the
community according to equation (3.5), which allows us to determine the
radioactivity of the organisms C^-/W-j individually as a function of time
and use it as a control to estimate the reliability of the parameters
used in the model (Shushkina et al . , 1974; Shushkina, Kislyakov, 1975).

We can also use the method of mathematical modelling based on
equations (3.1-3.5) and the parameters which they include, in
combination with physiologic methods, to estimate the rate of production
of individual trophic levels of zooplankton and calculate the net
production of zooplankton and of the planktonic community as a whole
(Vinogradov et al . , 1976). In estimating the intensity of production of
populations of aquatic animals and individual trophic groups (levels)
using the balance equation (3.5), we must have some idea of the spectrum
of feeding of the animals studied, their trophic connections, rates of
consumption of food C and its assimilation U"^ as a function of the
concentration of the food. These parameters are rather well known for
fresh water, less well known for marine planktonic communities,
particularly in the tropics. Nevertheless, the experimental and field

297

observations allow us to produce not only a qualitative, but even a
quantitative description of the trophic relationships in marine
planktonic communities. Based on the available materials (Jergensen,
1955; Mullin, Brooks, 1967; Zaika, Pavlovskaya, 1970; Pavlova et al . ,
1971; Petipa et al . , 1971, 1974, 1975; Zhukov, 1974; Sorokin, 1974f, g;
Sameoto, 1974; Barna, Weiss Dale, 1974; Swale, Belcher, 1974; and
others) it is possible to construct a system of primary trophic
connections of the community of the Sea of Japan and the equatorial
region of the Pacific Ocean (Shushkina et al . , 1974) and to estimate the
feeding selectivity coefficient I^j (Shushkina, Kislyakov, 1975;
Vinogradov et al . , 1976).

The rate of consumption C^-j of food at the jth level (group) by
organisms of the ith level (group) as a function of its concentration
can be described by the following equation (Ivlev, 1955; Winberg,
Anisimov, 1969; Petipa et al., 1971):

'"Pax ,, _ -?*i

\

Cij = C'ij (1 - e-^-^iJ), (3.6)

where c is a coefficient which is assumed to be close to 1.0, X ^^ is
the tropho-ecologic coefficient (Menshutkin, 1971). The value of the
maximum diet of the ith group consuming the jth group Ct^j is determined
on the basis of the maximum diet of species of the ith group, including
all types of food cf ^ and the fraction which the biomass of the jth
group represents in the total biomass of food, considering feeding
selectivity (Shushkina, Kislyakov, 1975; Vinogradov et al., 1976). The
quantity Ct' can be described (Winberg, Anisimov, 1969) on the basis
of the cost of metabolism R and the maximum possible increase, given
that metabolism P , based on equations (3.1) and (3.5):

,max /ninax

..max
K2

Cr = (Pi + R)-Uniin = R(— ^ + D-Umin- (3.7)

1-K2

3.3 Estimate of Production of Populations, Trophic Levels,
Zooplankton and the Planktonic Community as a Whole

Based on equations (3.1-3.7), we can estimate the intensity of
production--the mean daily P/B coefficients--for individual populations,
for trophic and systematic groups of planktonic animals, for all
zooplankton, and for the planktonic community as a whole.

The estimate of mean daily P/B coefficients for various groups of
marine tropical plankton, performed by a physiologic method, is
presented in Table 14. The initial data for calculation, obtained in
the western Pacific (44th and 50th cruises of the VITYAZ') allow us to
determine the range of change of P/B coefficients with the most probable
values of K2 (0.3-0.4) within limits of dimensions of animals for which
the energy equivalents (W = bl*") and metabolic rate (R = aWM have been

298

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299

measured. The mean daily P/B coefficients for most mesoplanktonic
animals have been found to be 5-15%, corresponding to the data of other
authors (Greze, 1971, 1973a, b; Malovitskaya, 1971, 1973). It should be
emphasized that the physiologic method using values of Ko constant for
the entire population and ignoring the specifics of the food, the
pressure of predators and other factors which influence the values of
production, can produce only approximate values of production and P/B
coefficients. A more precise estimate of the level of production can be
obtained by combining the physiologic and radiocarbon methods with
mathematical modelling in experiments in situ. This type of estimate
has been made for the planktonic animals of the Sea of Japan (Shushkina
et al., 1974) and the equatorial region of the eastern Pacific
(Shushkina, Kislyakov, 1975). The results of the determinations (Table
15) in some cases were close to the values determined by other methods,
for example for the copepodites of Calanus plumchrus (Parsons et al . ,
1969) and the chaetognaths (G. N. Mironov, 1970, 1973; Zaika, 1969).
However, most of the determinations differed significantly from the
values produced earlier for closely related animals (Greze et al., 1968;
Malovitskaya, 1971, 1973). Since the P/B coefficients which were
compared were produced by different methods for different species of
animals differing in their size and conditions of life, close similarity
of the P/B coefficients should not be expected.

It is thought that the intensity of production depends on
temperature conditions, since they determine the growth rate and
breeding rate of animals (Mednikov, 1965; Zaika, Malovitskaya, 1967;
Reeve, 1970; and others), the availability of food (Winberg et al . ,
1965; Shushkina, 1966; Menshutkin, 1971) and the dimensions of the
animals (Zaika, 1972). This last variation--the increase in rate of
production with decreasing size of the animals--is, apparently, general
in nature.

The results of estimation of the intensity of production of
populations and individual systematic groups of planktonic animals do
not allow us to make a judgement concerning the rate and intensity of
production of entire trophic levels, of zooplankton and of the plankton
as a whole, which is most important in the study of the production
characteristics of aquatic communities. Very few estimates of this type
have been made for marine plankton (Mednikov, 1960; Petipa et al . , 1970;
Greze, 1970, 1971, 1973a; Vinogradova, Gruzov, 1972; Shushkina,
Kislyakov, 1975; Vinogradov et al . , 1976; V. D. Fedorov, 1970).

As an example, let us present the results of estimation of the
productivity of various levels of the planktonic community in the upper
(0-150 m) layer of water in the equatorial region of the eastern
Pacific, obtained by combining the physiologic method with mathematical
modelling [equations (3.1-3.5)]. The material was collected during the
17th cruise of the AKADEMIK KURCHATOV in 4 measurement areas with
trophicity decreasing from east to west. The planktonic community was
subdivided into: phytoplankton, bacteria, protozoa and mesoplankton.
The phytoplankton was subdivided into small (cell diameter < to 15 urn,
volume < 1,000 \sn^) and large (diameter > 15 m, volume > 1,000 pm^) .
The bacteria, which represented a single trophic level in our example,

300

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301

included dispersed forms and aggregates (diameters > 4-5 pm) . The
protozoa, belonging, probably, to at least 2 trophic levels, were
subdivided into small heterotrophic flagellata (diameters - 3-5 pm) ,
feeding on small phytoplankton and dispersed bacteria, and infusoria,
feeding on phytoplankton, bacteria and flagellata. The mesozooplankton
was subdivided into 2 trophic levels: omnivores with primarily filter-
type feeding, consuming phytoplankton, bacteria and protozoa and
catching predators, consuming infusoria, omnivores and animals of their
own level. The omnivores included: fine filter feeders (appendicularia
and doliolids), the primary food of which consisted of small
phytoplankton, bacteria and flagellata; small copepoda (nauplii,
copepodites of copepoda and mature calanoida measuring up to 1 mm),
feeding on phytoplankton, aggregated bacteria and protozoa;
nonpredaceous large calanoida (Undinula, Eucalanus, Nannocalanus, etc.),
consuming phytoplankton, aggregated bacteria and infusoria. The
mesoplanktonic carnivores were represented by: cyclopoida, the food for
which consisted of the infusoria, fine filter feeders and small
copepoda; predaceous calanoida (Euchaeta, Candacia, etc.), feeding on
fine filter feeders, small copepoda, and cyclopoida; other carnivores
(primarily chaetognatha, polychaeta and hyperiids), consuming all
omnivores, cyclopoida and predaceous calanoida.

The rate of production of the lower trophic levels (phytoplankton
and bacteria) decreased with decreasing trophicity of the water from 18
(phytoplankton) and 6.6 Kcal/m^*day (bacteria) in the zone of most
intensive upwelling (97°W) to 3.2 and 2.3 Kcal/m^-day at 140°W. For the
mesozooplankton, and particularly the predaceous forms, this decrease
was less strongly expressed. For example, for the cyclopoida, the rate
of production decreases from 0.7 to 0.1, while for all predators except
copepoda, it decreases from 0.4 to 0.1 Kcal/m'^'day. The specific
production (mean daily P/B coefficients) for the phytoplankton and
bacteria increase as the water becomes poorer, decreasing for the
protozoa and mesozooplankton.

It has been repeatedly stated that a young community, forming in
the eutrophic waters of an upwelling, accumulates energy, and then, as
the community develops, the water "ages" and the trophicity decreases,
the energy is expended (Vinogradov et al . , 1971). The data obtained in
the equatorial eastern Pacific allow us to explain the mechanism of this
process. As we move from east to west along the zonal component of the
surface equatorial current, the trophicity of the water and biomass of
all primary groups of microplankton and mesoplankton decrease,
particularly that of the phytoplankton and bacterioplankton. The degree
of satisfaction of the food demands decreases, the stress of trophic
connections increases and the effectiveness of energy transfer through
the system increases. The significance of predators increases, and
cannibalism increase, both within groups of protozoa, and within groups
of predaceous mesozooplankton--from 50 to 80% of the production of
zooplankton and almost all of the production of protozoa are consumed by
individuals at the same trophic level. As a result, the total and
specific daily production of these groups and of all zooplankton take on
negative values. The very expenditure of energy mentioned above
actually occurs. True enough, the trophic pressure on phytoplankton and

302

bacteria is decreased in this process, which may result in a renewed
increase in production of the entire community. We found this at
155°W. Apparently, the net production of the community undergoes
significant, regular fluctuations against a background of overall
reduction. Probably, changes in the production of the community occur
analogously as it develops in other regions of the ocean.

Thus, the materials accumulated to date give us some idea of the
production of populations of marine planktonic animals, of trophic
levels of zooplankton and of the planktonic community as a whole.
However, as we have noted, due to the paucity of factual material, it is
difficult to draw any broad conclusions concerning the intensity of
production of planktonic animals and zooplankton in general in waters of
different trophicities and in different geographic zones of the World
Ocean. However, we can hope that the problem of efficient utilization
of the resources of the World Ocean which has now arisen will lead in
the next few years to rapid development of studies of the process of
production in marine communities, allowing us to develop descriptions of
these processes for the entire World Ocean and for its individul parts,
thus approaching a solution of the problem of prediction and even
control of the productivity of marine ecosystems.

303

4. Production of the Zoobenthos .
(A. N. Golikov, 0. A. Skarlato)

Estimation of the production of the macrozoobenthos involves a
number of methodologic difficulties. It is very difficult to obtain
reliable information on the quantitative distribution of organisms of
the benthos. On hard bottoms and in stands of underwater vegetation,
determination of the quantity of organisms using the standard equipment
for quantitative measurement (trawls, drags, bottom diggers) yields
results which are low by tens or even hundreds of times (Barnes, 1962;
Skarlato et al., 1964), while in soft bottoms the results of the use of
these devices will still be low by several times. The significant error
in information obtained by standard quantitative benthos-counting
devices from ships in comparison to the actual picture has even led to
the use of the term "bottom-digger benthos". More reliable data on the
quantitative distribution of the benthos can be achieved by quantitative
methods of hydrobiologic research using divers (Golikov, Scarlato, 1965;
Golikov, Scarlato, 1967). This method is based on direct counting of
organisms in homogeneous areas of biotopes covering areas varying from
100 m down to 20 cm^, depending on the dimensions of the organisms in
question and the nature of their distribution. Organisms are counted in
areas, the dimensions of which vary on a logarithmic scale (100, 10, 1,
0.1 nr-, etc.) corresponding to the logarithmic distribution of organisms
in biocenoses. The selection of sectors for sampling is performed by
research divers, who directly (visually) estimate the degree of
homogeneity of biotopes, the boundaries of biocenoses, the abundance and
variety of life. This makes the quantitative method using divers
relatively reliable and accurate as a method of studying the marine
benthos in the upper levels of the shelf, down to depths of 30-40 m. At
greater depths, in parallel with the use of trawls and bottom diggers,
it is desirable to utilize underwater photography and television.

To determine the production and bioenergetics of biocenoses, one
must study the production of the specific populations in these
biocenoses. Obviously, reliable determination of production is
impossible without knowledge of the peculiarities of growth and duration
of life of the animals of a given biocenosis. Most significant for the
determination of the production properties of populations is the study
of the growth rate and duration of life not of individuals, but of the
majority of individuals in a population. However, reliable
determination of the age of individuals is usually possible only by
means of cumbersome observations in cages.

The general regularities of growth of poykilothermic aquatic
animals and methods of its determination are well known (Vinberg, 1968;
Vilenkin, Vilenkina, 1973; Alimov, Golikov, 1974; and others); we shall
discuss only 1 method of estimating the group growth of macrobenthic
animals.

304

Determination of the group growth of individuals can be based on
analysis of the dimensional and weight structure of a specific
population which, in species with intermittent (not year-round)
breeding, has generative discreteness (Golikov, 1970). Since in the
temperate and high latitudes, practically all species of marine animals
have intermittent breeding due to the elevated stenothermicity of
gametogenesis and the early stages of ontogenesis (Kinne, 1970), the
method of determination of the group growth and age of individuals on
the basis of generative discreteness in the structure of populations is
a universal one. When this method is used, one must first consider not
the frequency of occurrence of individuals of a given dimensional class,
as in determination of growth on the basis of the Petersen distribution
or the probability paper method, but rather the distribution of
individuals by actual dimensions, i.e., the presence or absence of
individuals of a given size at the moment of observation. It is
methodologically important to analyze the dimensional distribution of
individuals based on materials collected over a relatively short time
interval, so that the change in dimensions of individuals during the
process of growth will not mask the generative discreteness in the
structure of the population.

It is characteristic that individual variations in the growth rate
of individuals within a generation, as a rule, do not exceed the
differences in dimensions of groups of individuals of successive
generations. This results from the unity of the gene pool of the local
population, the polygenous determination of individual variability of
growth and the similarity of phenotypic shifts in the growth rate for
all members of a population under the influence of identical
conditions. The variability in growth rate of individuals of one
generation is greater in species with an extended breeding period than
in those with short spawning times. Individuals born at the beginning
of a breeding period grow more rapidly, survive better and achieve
greater dimensions than individuals appearing near the end of the
breeding period, which are subjected to the unfavorable effects of
temperature in similar phases of ontogenesis (Golikov, 1975b).

Due to the asymptotic nature of growth of the overwhelming majority
of marine benthic organisms, differences in the dimensions of
individuals in successive generations decrease with age. The method of
estimating the growth rate and age on the basis of the dimensional and
weight structure of populations is suitable for species which stop
growing in the later stages of ontogenesis, which usually is not
characteristic of poyki lothermic marine organisms. In this case, the
age of the oldest generations can be approximately determined on the
basis of the nonproportional increase in number of the last cohort: the
largest and oldest individuals having approximately the same
dimensions. Examples of generative discreteness in the structure of
local populations and determination of the growth rate and duration of
life of marine invertebrates on the basis of this characteristic have
been presented in a number of works (Golikov, Menshutkin, 1971; Golokov,
Menshutkin, 1973; Menshutkin, Golikov, 1971; Sirenko, 1973; Tabunkov,
1973, 1974; Menshutkina, 1975; and others), and are illustrated by data
on the structure of populations and growth of 2 species of gastropoda
with different life durations (Figs. 27 and 28).

305

/o ;z /¥ Iff /s zo zzHp

Fig. 27. Dimensional structure of populations of Mi noli a iridescens (a)
and Littorina squalida (b) during the summer in Pos'yeta Bay, Sea of
Japan. Ordinate shows number of individuals (N) per n&; abscissa shows
shell height, mm.

ears

Fig. 28. Linear growth of Minolia iridescens (a) and Littorina squalida
(b) in Pos'yeta Bay, Sea of Japan. Ordinate shows shell height (Hp),
mm; abscissa shows age, years.

The essence of determination of growth rate and life duration of
individuals in a specific population can be reduced to counting the
number of corresponding generations of discrete dimensional -wei ght
groups. In species with life cycles over 1 year in length, the first
dimensional -wei ght group, depending on the time of sampling and the
status of the population, corresponds to individuals born in the same
year, or individuals at least 1 year of age, while the second belongs to
individuals a year older, etc. With spawning in portions, extended
metamorphosis or the formation of spring and winter subgenerations,
individuals of a given year of birth form similar dimension and weight
groups, corresponding to the spawning peaks, and different from each
other in terms of dimensions and weight significantly less than
individuals of the previous year of birth. The reliability of
differences in dimensions of individuals of successive generations is
usully tested by statistical methods. In an analysis of the structure

306

of a population, it is important to have material covering most of the
ecologic zones inhabited by the species in the given location. This
allows us to consider individuals of different ontogenetic stages in the
population, frequently restricted to different biotopes. One simple
method of estimating the spatial heterogeneity of the dimensional
structure of a population is to compare the frequency of occurrence of
individuals of a given size in different sinusia (levels) of the
biotopes and at different depths.

The relationship between dimensional and weight characteristics of
individuals of a population is not difficult to estimate using the
equation W = aL , where W is the weight of an individual and L is its
maximum linear dimension. Studies of recent years (Alimov, Golikov,
1974; Tsvetkova, 1974; and others) have shown that the values of
coefficients a and b in representatives of a single life form do not
differ statistically. This greatly facilitates estimation of the
parameters of the equations for various species. The weight of
organisms of a single length (coefficient a) is determined by the shape
of the body and the specific weight of the organisms, while the
regression coefficient b is determined by the degree of allometry of
growth. In calculations of production, it is desirable to use the wet
mass.

In determining the production of the zoobenthos, most authors use
various modifications of the Boysen-Jensen method (Boysen-Jensen, 1919),
based on estimation of the total weight increase of individuals
remaining in the composition of the population over the period of
observation and the main weight of individuals eliminated during that
time. In the simplest case, the annual production of a population is
calculated by the equation: P = Bx + B^, B^- and B^+i are the
biomass of a population at the beginning and end of the year analyzed,
Bg is the biomass of individuals eliminated during the year, estimated
as the difference between the initial and final populations, multiplied
by the mean weight of individuals eliminated:

This method, sometimes with slight variations, is widely used in the
literature to calculate the production of massive species of zoobenthos
(Boysen-Jensen, 1919; Blegvad, 1928; V. V. Kuznetsov, 1941, 1948a-c;
Vorob'yev, 1949; Shorygin, 1952; Sushchenya, 1967; Masse, 1968;
Khmeleva, 1973; and others). It is usually used for littoral regions,
located near marine biologic institutions, since determination of
production by this method requires repeated frequent sampling of
materials from the same biocenoses. In the improved Boysen-Jensen
method (Bekman et al., 1968; Winberg et al . , 1971; and others),
production is calculated by the equation:

P = I 7 (Nt + Nx+l) (Wt+1 - Wt) "Sf . (4.2)

T=0

307

where N is the number of age groups. At is the time sector analyzed.

Considering that in a stable population (one in which upon
completion of a generative cycle, the initial dimension-age structure
and population are restored) of multiannual benthos organisms, the
annual production (P) is equal to elimination (E), production can be
estimated by the equation:

P = E = I ^ (W, + W,+i) (N, - N^i) -^ , (4.3)

T=0

reflecting the mean weight of individuals eliminated from the population
over the time of observation. To determine the annual production, the
results of observations for individual sections of time are added.

Obviously, the accuracy of calculation of production will be
higher, the more frequently observations are performed. This results
from the need for the most accurate possible determination of the time
of elimination of individuals in various age groups and the appearance
of replacements in the new generation or by migration. If the sampling
frequency is too low, the weight gain of individuals which disappeared
from the population long before the moment of observation may be
included in production, leading to an elevated calculated value of
production or, conversely, lack of data on the time of supplementation
of a population will lead to reduced values. Naturally, one must be
sure that the calculation of production is performed for the same
population studied at the beginning of observations.

Considering the methodologic difficulties, a number of authors have
suggested that the daily growth of individuals or specific P/B
coefficients of populations obtained experimentally or by mathematical
calculation be used to calculate production (Konstantinov, 1967, 1970;
Zaika, Malovitskaya, 1967; Greze, 1967, 1973a, b; Mathews, 1970; Zaika,
1972; Burke, Man, 1974). However, it is obvious that the P/B
coefficients or cumulative daily growth of individuals in different
generations depend greatly on the relationship of the populations of
individuals of different ages and the conditions of existence of
populations and, consequently, are essentially different during
different seasons of the year and in populations living under different
conditions. This once more emphasizes the need to take samples as
frequently as possible in order to allow estimation of changes in
population and the weight of individuals in various cohorts.

Calculation of the production of populations of benthic animals can
also be performed on the basis of the ecologic-physiologic approach to
estimation of the weight increase of individuals, which is dependent on
the intensity of their metabolism. The production is calculated on the
basis of the ratio of the growth of individuals to the cost of
metabolism, which is expressed by the equation for the coefficient of
net production, or the effectiveness of utilization of assimilated food
for growth: K2 = P:(P + R), where P is the production (cal), R
represents the cost of metabolism (Winberg, 1966, 1968; Bedman et al.,

308

1968; McNeil, Lawton, 1970; Klekowski, 1970; Hughes, 1970; Bregman,
1971; and others). After calculating the value of K2, it is not
difficult to determine the production of individuals of various sizes
(weights), then the production of the population, as the sum of the
growth of all individuals present in the population during the time of
the analysis. Obviously, to analyze the annual production of a
population by the ecophysiologic method, it is also necessary to know
the relationship of the numbers of individuals in cohorts during various
seasons of the year, particularly since the rate of elimination and
intensity of metabolism and growth of individuals change greatly from
season to season.

As we can see, all of the methods analyzed above for calculation of
production require regular, year-round observations of changes in the
numbers of individuals of various ages. These observations of
populations of benthic organisms are frequently impossible, particularly
in areas far from scientific research institutions. Considering this
fact, as well as the difficulty of tracing the dynamics of the
populations of organisms in the open seas, a static-dynamic method of
determination of production has been suggested, based on analysis of the
size-weight and age structure of populations at the moment of
observation as a result of the annual production process (Golikov,
1970). The method is based on the fact that the structure of a
population is used to establish the growth rate and age of individuals
(with a check on the basis of morphologic indications of growth, if
there are such), after which the quantity of living matter produced by
the population during the year before the time of analysis of its
initial state (growth production of population Pg) is calculated by
estimating the weight gain of all individuals detected at the moment of
observation, using the equation:

Pg = I N,(W,+i - W,) ^ (4.4)

T=0

or the classical equation (4.2).

The value of At in the version analyzed is equal to one year.
Based on equation (4.4), the weight gain of all individuals surviving
and those eliminated during the time period analyzed is calculated,
while equation (4.2) is used to determine the weight gain of all
individuals surviving and half of those eliminated during this period of
time. Obviously, with a sharp decrease in the population of the
generations at the beginning of the time sector analyzed, with
relatively uniform elimination, and in those cases when the time of
elimination of individuals is not known, the best result will be yielded
by an estimate of the growth production using the equation generally
used for this purpose (4.2). However, in those cases when most of the
elimination occurs at the end of the time sector analyzed (for example,
elimination after spawning), calculation of growth production by
equation (4.4) may be more accurate.

Determination of growth production of a population using a single
sample per year is based, as in calculation of production by the other

309

methods analyzed above, on the idea of the relative stability of natural
populations of annual species where there are stable, periodically
repeating fluctuations in the environmental conditions. Actually, the
supplementation of a specific population with juveniles is usually
observed in a given area at a constantly defined time; for many species,
at this same time, we observe the post-spawning elimination of older age
groups, and the population also decreases during the winter. All of
this leds to fluctuations in the numbers of various cohorts in the
population which are predictable with respect to time, allowing us to
assume that during different years, at the same time of year, the
population has approximately the same number of individuals and total
biomass, with a similar relationship of numbers of individuals of
various generations. The steady nature of many natural populations and
the comparability of values of growth production calculated for a given
season can be shown on the example of analysis of the production process
in populations of a number of species of benthic organisms in Pos'yeta
Bay (Golikov, 1970; Golikov, Scarlato, 1970; Golikov, Menshutkin,
1973). A disruption of the steady nature of populations is observed
upon sudden, aperiodic changes in environmental conditions, related to
natural processes or human interference. Obviously, the closer the
population being analyzed is to a steady state, the more precisely the
calculation of its growth production can be performed, using a single
sample. In a steady population, increase and elimination in all
generations occurs at approximately the same time, and restoration of
near-initial structure in each generation is achieved by the growth of
the surviving individuals of the younger generations (supporting a
portion of the production process). The very phenomenon of steadiness
results from the presence of compensatory processes to replace losses in
populations and elements of self-regulation in population dynamics.

The method we have presented for calculation of the annual growth
production of a steady population allows us to abstract ourselves from
seasonal, functional and random changes in growth rate and rate of
elimination of individuals, and reflects the quantity of living matter
formed during the course of the year (at the moment of observation),
necessary for creation of a definite dimension-weight and age structure
of the population. It allows us to determine the approximate annual
growth production of the population based on a single, rather complete
quantitative sample, if it is impossible to perform constant, year-round
observations. The possibility of determining production on the basis of
a single reliable quantitative sample of a population is also reported
by G. G. Vinberg (Bekman et al . , 1968, page 100). With simultaneous
analysis of a population and estimation of the production on the basis
of a single sample, the only significant factor is the time of
disappearance of individuals from the population, since the weight
growth of individuals which have moved into the subsequent age group is
automatically considered. If we know the spawning time and the time of
supplementation of the population with juveniles for the species of a
given biogeographic complex, as well as the general regularities of
elimination, we can determine the most probable periods of elimination
of individuals of the population and introduce the corresponding
corrections.

310

A model experiment to analyze the accuracy of estimation of
production by this method has shown that the determination of the mean
annual growth production of a population based on a single sample is
rather reliable and accurate, if the time of collection of the materials
is adjusted approximately to the middle of the period of supplementation
of the population with juveniles (Golikov, Menshutkin, 1971). In
temperate waters in the northern hemisphere, this is usually observed in
the summer or early fall. This conclusion has been confirmed by
analysis of seasonal changes in the production process of a number of
species of gastropoda, differing in their biogeographic distribution and
duration of life (Golikov, Menshutkin, 1973; Golikov, 1975b).

In cases when observation of the structure of a population is
performed at a time which is not favorable for determination of the
annual growth production (peak of supplementation with juveniles or
maximum of elimination), the growth production calculated up to this
time may differ greatly from the mean annual growth production (by up to
80%). However, 2 samples, taken at an interval of approximately 1/2
year, allows the possible error to be decreased to less than 25%, while
4 observations during the various seasons of the year allow the mean
annual growth production of a population to be estimated with an error
of less than 5% (Golikov, Menshutkin, 1971). If it is possible to
observe the structure of a population during various seasons of the
year, the mean annual growth production can be defined as the mean of
the annual productions calculated for each moment of observation (Pg,-):

n

•^1 Pgi
p„ =IiL_lL (4.5)

•^gm n

where n is the number of observations.

Obviously, of greatest interest is observation of the full
production of a population, including all living matter produced during
the course of a year. The total production of a population must include
all of the juveniles produced during a year. The total production of a
population can be approximated, depending on the nature of elimination,
by one of the following two equations:

" 1 1

P = NqWo +Jq^ (N^ + Nx+l) (Wx+1 - W^) ^ (4.6)

or

P = NqWo +Jq N, (W,+i - W,) ^ . (4.7)

where NqWq is the biomass of individuals of a given year of birth.

311

The production of a population includes both the weight of
individuals which have disappeared from the population during the
calculated time due to natural death, consumption or migration, as well
as the weight gain of individuals remaining in the population at the end
of the period in question. Whereas the first portion of the production
process represents a sort of reserve of strength of the population, the
second portion is important in principle for its very existence. To
symbolize this second portion of production, which represents the
quantity of living matter formed during the time of turnover of a
generation (in this case--during a year) and remaining in the
population, the concept of supporting production has been developed
(Golikov, 1970). The supporting production P^ is responsible for the
creation of that portion of the biomass of a population which is formed
during the turnover of 1 generation. For species with a duration of
life of individuals of more than 1 year, the supporting production is
expressed as the sum of the biomass of juveniles (of the same year) and
the annual weight increase of the individuals of older generations
present at the beginning of the year.

n

= I Nx(W, - W,.i) 4 . (4.8)

T = 0

At

where W^ and Wx-i are the weight increase of individuals of the
generation in question, which survive and remain in the composition of
the population over the time interval analyzed (in this version--!
year). This same equation, with the corresponding time correction At,
is apparently suitable for estimation of the supporting production of
populations of species with durations of life of individuals of less
than 1 year.

It is significant that the production process during the course of
the time analyzed occurs in all generations of the population
simultaneously, which allows us to generate an integral expression for
the full growth production of the population and its supporting
component during the same time interval. The supporting portion of
production during the year preceding the time of observation, given
reliable data on the quantitative structure of the population and growth
of individuals, can be determined rather accurately using a single
sample, regardless of the degree of steadiness of the population, since
it reflects the weight increase of the surviving individuals of each
generation only.

If it is possible to perform several observations, the mean annual
supporting production can be determined using an equation analogous to
equation (4-5)

n

^ Psn
P -_ '-'\ . (4.9)

^m n

The supporting portion of the production process, not including the
living matter which has disappeared from the composition of the

312

population during the period of the change in generations, can be looked
upon as a characteristic reflecting the absolute weight increase of
individuals surviving through the year. The rate of growth and natural
duration of life of individuals are genetically determined and vary,
depending on the environmental conditions, only within limits permitted
by the genotype. From this standpoint, P5 is a genetically determined
characteristic of the population, resulting from the possibility of its
existence under the conditions in question with a mean duration of life
determined by the specific genotype and a fraction of individuals
surviving through the year determined by the population curve of
mortality and, obviously, showing selective preference.
Correspondingly, the value of P^ is the minimum of living matter which
can be formed during the course of a year, necessary for stable
existence of a population of a given age structure.

Naturally, the value of P^ is always less than the biomass of the
population, while the rate of turnover of matter (P^/B coefficient) is
related by a rigid, almost linear, inverse dependence to the age of the
individuals which predominate in terms of number, and is approximately
inversely proportional to the limiting duration of life of individuals
of the given population. In populations in which the age of most
individuals is < 1 year, the full cycle of living matter occurs in
approximately 1 year and P^/B =1. As the duration of life increases,
the value of the P^/B coefficient decreases proportionally. In species
which form several generations during the course of a year, the
supporting production must be correspondly greater than the biomass.
Since the mean age of individuals of a given population is determined
essentially by genotypic peculiarities of the species and changes
slightly during different seasons of the year, the value of the annual
P5/B coefficient, calculated for different seasons, fluctuates
insignificantly. Therefore, calculation of the mean annual value of
this coefficient on the basis of a single sample is rather reliable,
regardless of the time it was produced.

The rate of turnover of growth production of a population (Pg/B
coefficient) depends strongly on the relationship of elimination Tn
various generations and their relative numbers and changes significantly
(sometimes by several times) from season to seaon. The relationship
between the growth production of a population and its supporting part
depends on the age structure of the population. The greater the
relative share of juveniles and individuals of the younger age groups in
the population, the greater the Pg:Ps ratio and the greater the
prospects for the positive development of the population under these
conditions. Actually, young individuals with low biomass have great
potential for weight gain, and with a given level of elimination, an
increase in their number creates a reserve of reliability for continued
existence of the population.

If the total level of elimination is reduced, particularly in the
early, most sensitive phases of postlarval ontogenesis, and the survival
rate of individuals is increased (for example, by mariculture) , an
increase in growth production should occur, and as time passes, a
proportional increase in the number of surviving juveniles should result

313

in an increase in the biomass of the older age groups. The principle of
maximum increase in the population and survival rate of juveniles and
methods of its realization have been suggested for the conduct of
mariculture of a number of species of mollusks in waters of the Soviet
Union (Golikov, Scarlato, 1970).

In a steady population with a regular decrease in the number of
individuls as they grow, growth production of each generation is always
greater than the supporting production, due to the predominance of the
numbers of individuals in the younger age groups. If the steady-state
condition is disrupted in the direction of increasing the population of
the younger age groups, positive development of the population occurs
until the relationships between population and biomass of the various
generations achieve equilibrium at the new level and the relationship
between Pg and P^ is restored. Conversely, with a significant decrease
in the supplementation of juveniles, an increase is observed in the
share of supporting production, which may indicate that degradation of
the population is beginning. In those cases when supplementation of the
population is severely limited, supporting production may become equal
to growth production or even exceed it. In this case, one can expect
severe and extended depression or even disappearance of the
population. Actually, when supplementation of a population is reduced,
after a certain period of time has elapsed, a decrease occurs in the
number of producers, which, with a fixed level of elimination, causes a
still greater decrease in supplementation. A similar effect can be
observed in the case of a direct and sharp decrease in the population of
sexually mature individuals, leading to a significant decrease in the
effectiveness of spawning, for example, due to excessive fishing of
producer or sudden or unfavorable changes in the environment, usually
occurring along the edges of areas of distribution. A decrease in the
relative fraction of juveniles in the composition of these edge
populations of a species may frequently result from a sudden decrease in
the duration of temperatures favorable for breeding (Hutchins, 1947;
Golikov, Scarlato, 1973), which may even lead to total absence of
spawning in particularly unfavorable years. One result of this is a
decrease, at first in abiotic (Kinne, 1963), then in biotic potential of
the edge populations and a decrease in their growth production to the
level of the supporting production, or even below it.

At the boundaries of populations, the supporting production
apparently usully exceeds the growth production, which is one of the
mechanisms of limiting the area of distribution of a population. For
example, this phenomenon was demonstrated for a population of the
bivalve mollusks Nuculana pernula in Terpeniye Bay in the Sea of Okhotsk
(Tabunkov, 1974). Extensive information on the dynamics of the
population indicates that, given significant changes in the structure of
a population, the inertia of its development is very high and may
require many years for stabilization, or may result in cyclical changes.

The fact that the supporting portion of production is calculated
regardles of whether the population is steady or not allows us to assume
that the Pq/Pc ratio can serve as an indicator of instability of a
population and of the direction of its development (positive or

314

degrading), with a given nature of elimination. Determination of the
growth and supporting components of the production process allows us to
produce a quantitative estimate of the disruption of the stability of
the population which has already occurred, since a disproportion in the
population of various generations may result from variations in their
supplementation by juveniles and differences in the rate of
elimination. Analysis of the relationships between P_, P^ and the
biomass of the population can be of significant interest for
determination of the possible stable catch. Obviously, the catch in any
case must be less than the supporting portion of the production
process.

To illustrate the static-dynamic principle of calculation of
production on the basis of a single sample of a natural population, let
us present an example of simple determination of P„ (from the
calculation of the gradual elimination of individuals in successive
generations at the end of the analyzed time sector) and Pg, using
equation (4.8) (Table 16).

The structure of the local population of Buccinum cyaneium van.
tenebrosum, used as our example, from a region in the shallow eastern
portion of the Barents Sea by the south island of Novoy Zemli, a region
favorable for this form, reflects the status of the population in early
fall. Analysis of the dimension-weight structure of the population, in
combination with a study of the morphologic characteristics of growth,
form the basis of determination of the rate of linear and weight growth
and the duration of life of individuals of the species under these
conditions (Figs. 29 and 30). Calculation of the growth production (Pg)
and its supporting portion (P^) for the population in question showed
that the value of Pg was 62.5, of P^ — 46.5 g/m per year with a biomass
of 130.6 g/m^. Calculation of the production by this method can be
reduced (with some decrease in accuracy) by averaging the weight gain of
individuals of each generation over the year. As we can see from Table
16, the population in question is not stable (with a single level of
elimination, supplementation of the population with juveniles differs
from year to year), but is in a satisfactory condition, and, judging
from the ratio Pq/Ps ^ 1.34/1, has a sufficient reserve to support
continued existence.

The static-dynamic method was used to study the production
properties of a number of species of benthic invertebrates in many
regions (Golikov, 1970; Golikov, Scarlato, 1970; Golikov, Menshutkin,
1971, 1973; Sirenko, 1973; Tabunkov, 1973, 1974; Tsvetkova, 1974b;
Menshutkina, 1975; Yegorova, 1975). The results of these studies allow
us to analyze certain regularities in changes in the production process
of populations of a single species and biogeographically different
species in different sections in a body of water and in different
landscape-geographic zones. Species with similar characteristics of
dimensions and weight, in portions of a water area favorable for them,
have similar growth rate and life duration indices for individuals, and
frequently often comparable values of settlement density, rate of
elimination and production of each species. Naturally, the greatest
similarity with respect to these indicators is manifested by similar

315

Table 16. Calculation of annual production P and P^ of a population of
Buccinum cyaneum var. tenebrosum from the eastern portion of the Barents
Sea by a static-dynamic method based on one-time analysis of the status
of the population in early fall.

Ai;e ,

Shell

';ei;r.t of

P:>pula-

T

Vc.irs

H, m

Ir.dl-.idjals

tior. M,
Indiv./

s

S

g

g

0

3

0.4

0.4

0.4

0.4

1.1

1.1

9

0.45

0.45

0.45

0.45

1.2

1.2

10

0.3

1

0.5

1

1.3

2.6

11

0.55

0.55

0.55

0.55

1.4

1.4

1

18

0.8

1.6

0.8

1.6

2.2

4.4

19

0.85

0.S5

0.S5

0.85

2.3

2.3

20

0.9

0.9

0.9

0.9

2.6

2.6

21

0.95

0.95

0.95

0.95

2.85

2.95

22

1

1

0.9

0.9

3

3

23

1.3

1.3

1

1

3

3

24

1.5

1.5

1.1

1

3

3

2

30

3.5

3.5

2.6

2.6

2.1

2.1

30.5

3.8

3.8

2.8

2.8

2.1

2.1

31

4

4

3

3

2.2

2.2

3

35.5

5.6

5.6

2.7

2.7

2.9

2.9

37.5

6.7

6.7

2.6

2.6

3.3

3.3

i

40.5

8.5

8.5

2.7

2.7

4.5

4.5

41

9

9

2.9

2.9

5

5

42

10

10

3

J

4.5

4.5

5

46

14

14

4.5

4.5

3

3

49

17

17

3.5

3.5

3

3

6

50

IS

1

13

3.5

3.5

2

2

7

52

20

1

20

3

3

local

25

130.6

46.5

62.5

NOTE: ^Iq NW is the biomass of population B; AWs is the weight gain
of an individual of a given size during the current year (up to the
moment of observation); for individuals born that year, it is equal to
their weight, for individuals which were older, it is equal to the
difference between their weight and the weight of individuals one year
younger, calculated from the weight growth curve; NaWs is the production
of individuals present (not eliminated) of the given size in the year,
adding up to the supporting production of the population P^ for the year
up to the moment of observation; AWg is the expected annual weight
increase of individuals of a given size; for all individuals except
those having the maximum size in the population, it is calculated from
the curve of weight growth as the difference between the weight of
individuals of a given size and the individuals a year older; NAWg is
the production of individuals present and eliminated of a given size
over the course of the year, while in some it represents the growth
production of the population P over the year in question up to the
moment of observation. ^

315

IZ

16

ZO ZU Z8 SI

SS

^O

^■^

«^ 5Z Up

Fig. 29. Dimensional structure of a population of Buccinum cyaneum
tenebrosum in early fall in the eastern portion of the Barents Sea.

/d;

Ordinate shows number of individuals N per
height H , mm.

abscissa shows shell

W.

20

//
8

♦ - 8 -

^ Years

Fig. 30. Linear (1) and weight (2) growth of Bucci num cyaneum var.
tenebrosum in the eastern Barents Sea. Ordinate shows weight (W^),
and shell height H mm; abscissa shows age, years.

species and genera wi
from the similarity o
population, biomass a
organisms with short
with large dimensions
particularly with ape
the unevenness of the
life form, the fluctu
greater than under re

th similar dimensions and body weights, resulting
f their metabolic activity. The fluctuations in
nd production of populations are maximal for small
life cycles and comparatively greater for species

and longer life durations. With severe, and
riodic changes in environmental conditions due to

rate of elimination of species even of a single
ations in the production process are significantly
latively stable conditions.

The rate of the production process is related to the genetically
determined thermopathy of the species. In species of warm-water origin
in the northern hemisphere, the maximum production is observed in the
southern portion of their areas of distribution in shallow waters and
becomes quite great during the heat of summer. The mean annual value of
production of these species in boreal waters can be calculated on the
basis of observations made in early fall. The widespread boreal species
in the southern portions of their areas of distribution yield the
maximum production in spring, and reach the mean annual values of their

317

production in early summer; in the central and northern portions of
their areas of distribution the maximum production is shifted to the
heat of summer, approaching the mean annual values in early fall. In
Arctic waters, boreal-arctic species yield the maximum production at the
end of hydrologic summer. Some high Arctic and Antarctic species show
their maximum production in winter.

In water areas differing in their physical and chemical modes, the
production process in populations of the same species occurs
differently. Its rate increases with an increase in temperature (within
the limits of the optimum for each species), while the degree of
fluctuation increases with an increase in the variability of natural
conditions. Thus, in the inlets of Pos'yeta Bay, a number of relatively
warm-water low-boreal species reach their maximum production in
midsummer, while in open areas of the bay, the maximum is reached only
in the fall (Golikov, Menshutkin, 1973). Species which are subtropical
in origin achieve high production in the boreal waters of the Pacific
only in shallow inlets which are thoroughly heated in the summer (even
if they are quite remote from each other), and are encountered only as
individuals or are completely absent in nearby open, colder sections.

It is clear that in order to understand the biologic processes
occurring in marine ecosystems, we must do more than study the
production capabilities of populations of leading species, or even of
entire biocenoses. In order to study the regularities of the cycle of
biologic energy in ecosystems of various types, we must know, as a
minimum, the consumption of food (C) and its assimilation (1/U) for the
various trophic levels, the cost of metabolism (R), the effectiveness of
utilization of consumed and assimilated food for growth (K^, K2) and the
flow of energy through the population, or the assimilated energy (A =
P + R). In the literature, a tremendous quantity of information has
been accumulated on these parameters for marine benthic organisms. Data
are also available on the calorie content of various groups of marine
invertebrates and algae in sufficient quantities for measurement of the
biologic processes in identical bioenergetic units — calories. Most of
the coefficients necessary for calculation vary within relatively narrow
ranges. Thus, for most of the organisms studied, the assimilation of
food is usually 60-80% of the diet, the regression factor in the
equation of metabolism as a function of weight (R = aW ) averages 0.75-
0.80 (Hemmingsen, 1952; Vinberg, 1966). The coefficient of
effectiveness of utilization of assimilated food for growth is
approximately the same for species with similar dimension-weight and age
structures in a given landscape-geographic zone, averaging 0.3-0.4 for
populations of macrobenthos in temperate waters. In species in the
higher latitudes, this coefficient increases significantly due to the
greater quantity of lipids in the food, with their high energy capacity
(Golikov, 1975a, b) . Of particular interest for an understanding of the
trophodynamic relationships in benthic biocenoses is the study of the
ecologic effectiveness of populations. This characteristic is
calculated as the ratio of production of a population at the ith trophic
level to the production of populations of the i-l-th level, consumed by
them and, as Lindeman has shown, this characteristic averages about
10%. Preliminary calculations of the transformation of energy in the

318

benthic biocenoses we have studied yield results which do not differ
greatly from this quantity.

In connection with the above, it is obvious that the greatest
difficulty in the study of the transformation of biologic energy in
marine ecosystems is represented by empirical determination of the
growth of individuals and the production of specific populations under
their conditions of existence. However, due to the similar reaction to
changing environmental factors of different specific genotypes formed
under identical conditions (Golikov, 1973, 1975b), the production and
bioenergetic potential of species with comparable dimension-weight
characteristics under analogous conditions change in parallel. This
makes modelling of the production process of populations in natural
ecosystems possible, if we know the conditions of origin, density of
population and weight characteristics of the species making up the
populations.

319

CHAPTER V. MATHEMATICAL MODELLING OF THE FUNCTIONING
OF A PELAGIC ECOSYSTEM

Analysis of the environment and its population as a single,
interconnected system has been one of the most fruitful ideas of modern
ecology, opening broad doors for the systems approach to the study of
biologic processes in the biosphere. From this standpoint, the ocean
and its population can also be looked upon as a single, dynamic system
(Lebedev et al., 1974).

The systems approach has allowed the ideas, methods and apparatus
of such mathematical disciplines as cybernetics, information theory,
game theory and decision theory to be applied to the study of biologic
phenomena. However, in order to actualize the capabilities of these
disciplines, information on the structure and functioning of biologic
objects, communities in the present case, must be summarized and
formalized, and used as the basis for the construction of a model. This
requires that only the basic, definitive, parameters and connections of
the system be used, ignoring many interesting details. Unavoidably,
this leads to some internal protest among researchers who have spent a
great deal of time and effort in the study of details.

Depending on the nature of the task at hand, the degree of
development and specifics of the mathematical apparatus used for its
performance and the completeness of the information available on the
object of study, various models can be used: for example, description
of processes by differential equations (deterministic models), analysis
of random processes (stochastic models) or the development of algorithms
of self organization (self-organizing models). However, in any case, a
model should describe the complete set of elements present in the system
and their interactions, and should allow evaluation of certain
situations arising in the actual systems which either cannot be directly
measured or can be measured only with great difficulty.

Obviously, so-called "simulation models," allowing the use of
computerized numerical models to draw conclusions concerning the
behavior of a system as its various parameters change, and even allowing
decisions to be made concerning the most effective methods for more
traditional study of the system (Menshutkin, 1972), are of particular
prognostic value. Furthermore, the construction of such models is an
important means for testing the agreement of individual experimentally-
observed facts. Simulation models are closely related to imitation
models, differing in that they do not include a portrait description of
the object due to the insufficiency of initial data on the object.
These models can describe both the functioning of biologic systems and
their structural peculiarities, for example the regularities of
formation of horizontal (Wroblewski et al . , 971; Wroblewski, O'Brien,

320

1976) or vertical nonuniformities in the distribution of plankton
(Vinogradov et al., 1972; and others).

Another, basically different, type of model is the analytic model,
used for qualitative analysis of the general characteristics of
ecosystems related to estimates of their variety, stability, etc.

In what follows, we shall analyze several approaches to the
modelling of marine ecosystems and their components.

321

1. Simulations of the Functioning of a Pelagic Ecosystem.
(M. E. Vinogradov, V. V. Menshutkin)

The functioning of marine communities is determined by a complex
set of relationships between populations, based on evolutionary
adaptation of organisms to existence under the conditions of the system
in question. The morphophysiologic peculiarities of the organisms,
their genetic characteristics, behavioral reactions, etc., play a
definite role in this process. Various types of connections arise
between the components of communities, but it can be considered that the
basic connections in communities, integrating them and defining the
basis of their structure and productivity, are food connections (Elton,
1946; Vinogradov, 1970b; and others). Therefore, the study of trophic
relationships within a community, estimates of the flows of energy
through the biologic system and its utilization by the various trophic
groups, yield the most essential information concerning the functioning
of communities.

For aquatic, and particularly pelagic, communities, the energy
principle of investigation is especially effective. The significant
homogeneity of the biotope determines the leading role of trophic
connections in the regulation of the development of the aquatic
ecosystem as a unit whole. Connections which are not directly related
to feeding play a distinctly secondary role in oceanic pelagic
ecosystems, in contrast to marine benthic and, particularly, terrestrial
ecosystems. From this standpoint, pelagic ecosystems are the simplest
for modelling and at the present time, probably, it is only for these
systems that we can attempt to construct a sufficiently complete model
of the balance relationships. Furthermore, the abiotic conditions,
which directly effect the functioning of the community, can be
quantitatively estimated with ease for the pelagic zone.

The study of the energy characteristics of the population of the
deeper levels, requiring experimental observation, as yet encounters
significant methodologic difficulties; therefore, we must limit
ourselves to analysis of the communities of the surface (productive)
zone. These communities include practically all of the phytoplankton
and about half of the zooplankton of the waters of the ocean and, in
fact, determine the productivity of the ocean. The study of their
functioning is of singular theoretical and practical interest.

1.1 Statement of the Task of Modelling of Balance Relationships in
Oceanic Pelagic Ecosystems

The construction and investigation of mathematical models of the
functioning of pelagic ecosystems has a rather long history (Patten,
1968). The following works are probably among the most interesting:
Riley et al . (1949), Steele (1962, 1974), Vollenweider (1965), Dugdale

322

(1967), and Gushing (1959a, 1969). In the Soviet Union, the works of G.
G. Vinberg and S. A. Anisimov (1966) and of A. A. Lyapunov (1971), have
been significant in the development of mathematical modelling of aquatic
ecosystems.

The approach of A. A. Lyapunov to the modelling of complicated
systems (Lyapunov, Yablenskiy, 1963) is similar in its general features
to the macroscopic method of H. T. Odum (1971). The system is presented
as an assemblage of relatively independently functioning elements.
These elements are interconnected by various communication channels.
The role of signals passing through these channels may be placed by
portions of matter (energy) or information. Correspondingly, we can
distinguish material and information connections between elements of the
system.

One of the basic principles involved in the construction of
simulations of the functioning of ecologic systems is the principle of
conservation of matter and energy, which is interpreted in the form of
balance relationships for each (animate or inanimate) element of the
ecosystem. The mathematical model of balance relationships in an
ecologic system can be constructed only if a certain degree of
completeness has been reached in the study of the object being
modelled. In other words, we must have an idea of the distribution of
matter and energy among the corresponding elements, the regularities
which define the intensity of flows among the elements, what is included
in the ecosystem and what leaves or is removed from the ecosystem, and
in what quantities.

A. A. Lyapunov, in composing his model, assumed that all processes
occur without delay. This assumption, generally speaking, is not always
correct; however, upon transition to a discrete time step, one day or
more in length, the assumption of non-inertial elementary processes, for
example as concerns phy topi ank ton, is quite justified.

The model of A. A. Lyapunov contained merely six elements: light
(I), the concentration of nitrogen in assimilable ionic form (n^^), the
concentration of assimilable phosphorus (n ), the biomass of
phytoplankton (p), the biomass of zooplankton (f) and the concentration
of detritus (d). The following assumptions were made concerning each of
these elements: light is absorbed by the water (a), phytoplankton (a^),
zooplankton (a2) and detritus (a3). Nitrogen and phosphorus are
expended in the formation of primary production, in the process of
photosynthesis (coefficients h^ and hp) and liberated as a result of
decomposition of detritus (v^ and Vp). The intensity of photosynthesis
is limited by the light conditions and the concentration of nutrients.

Pp = mindl, gi^n^, QpHp), (1.1)

where z, g^ and gp are coefficients.

The consumption of phytoplankton by zooplankton is assumed to
follow Vol terra (coefficient e). The effects of multiplication of
zooplankton, consumption of detritus by zooplankton and the process of

323

cannibalism are considered analogously (coefficients y. , y„ and y^).
The natural mortality of the zooplankton ( e) and rate of vertical
migrations (w„) are also considered.

It is assumed that detritus is formed from dying zooplankton, and
also from zooplankton excreta, the quantity of which is proportional to
the quantity of food consumed (coefficients 6 , 6 , 6 ). The
phytoplankton does not die, but is completely consumed by the
zooplankton. The decomposition (g) and settling (cijo) of the detritus
are considered. The dissolved compounds of nutrients, phytoplankton,
zooplankton and detritus are carried in the vertical direction by
turbulent diffusion, the intensity of which is described by coefficient
K. The depth axis z is assumed to be directed from the surface of the
water downward.

The systems of equations of the model are therefore:

3Z

I (a + a^p + a2f + ajd). (1.2)

3P =
3t

%P

9f _
3t

y-^^p^

3d
3t

ef -

3nN a 3nw

-3t = -^NPpP^ V ^ ^(K-^)- (1-3)

3nn a 3nn

= YlPf - V'^ V^ -ef ^-3|(Kf) -^(.^f). (1.6)

ud + 6ipf + 62f2 + -^ (K If) - ^ (u)3d). (1.7)

Figure 1 presents a schematic diagram of one cell of the model.
The symbols used in the figure will be retained throughout this entire
section and serve as a language for the description of the structure of
the model of an aquatic ecologic system.

1.2 Model Simulating the Vertical Distribution of Elements of an
Ecosystem

The results of investigations carried out during the 44th and 50th
cruises of the VITYAZ' forced us to revise the model of A. A. Lyapunov
(Vinogradov et al., 1972; Vinogradov et al., 1973). The establishment
of a significant role of bacteria in the process of energy transfer and
the cycle of matter in the pelagic ecosystem (Sorokin, 1971a; and
others) forced a new structural element to be added to the model --
bacterioplankton. At the same time, it became necessary to consider the
transfer of energy from phytoplankton to bacteria by means of dissolved
organic matter (DOM). It was assumed that the excretion of DOM by
phytoplankton represented 30% of its production. The intensity of

324

o

-* 5

O^

l^-^

m

Fig. 1. Schematic diagram of a cell in the Lyapunov model. l--animate
element of ecosystem; 2~inanimate element of ecosystem; 3~group of
elements in a cell; 4--flows of matter; 5--trophic connection; 6--
transfer of matter; 7--energy of solar radiation; 8--information
connection; 9 — transport between cells; 10 — a cell of the ecosystem; I--
solar radiation; n|^--concentration of nitrogen; np--concentration of
phosphorous; Pp--production of phytoplankton; P--Diomass of
phytoplankton; f— biomass of zooplankton; d~concentration of detritus
(remaining symbols correspond to coefficients of equations 1.2-1.7 and
are explained in text).

multiplication of bacteria was limited by the concentration of nutrient
substances (detritus, DOM) and the limiting relationship of production
to biomass.

The next refinement of the model of A. A. Lyapunov occurred when
zooplankton stopped being considered as a single element, and became
divided into Protozoa (f^), microzooplankton (f2), fine filter feeders
(fo), coarse filter feeders (f^i), small predators--cyclopoids (s^),
other small predators--calanoias (S2) and large predators--chaetognaths
and polychaetes (so). The Protozoa included Flagellata (heterotrophs) ,
infusorians and radiolarians. The microzooplankton included the nauplii
of copepods; the fine filter feeders (less than 1 mm) included such
animals as the Oikopleura, Clausocalanus, Paracalanus, Acartia,

coarse filter feeders (greater
Scolecithrix, Neocalanus,

Lucicutia, small Ostracoda, etc.; the
than 1 mm) included Undinula, Pleuromamma,

325

juvenile Euphausiacea, etc.

Many experimental data on the variation in the intensity of feeding
of zooplankton with concentration of available food density forced us to
abandon the plan of Vol 'terra and begin use of the equation of V. S.
Ivlev (1955). According to this equation, the relationship between the
actual ration (C) and concentration of food (B) can be represented as:

C = Cn,axCl-e-?(B-B0)], (1.8)

where C„,^ is the maximum ration; Bn is the minimum concentration of

mdx , ■ 1 . u . - - . .
food, below which consumption ceases; C is a coefficient.

In establishing the selectivity of feeding in those cases when
direct experimental data were not available, it was hypothesized that
the concentration of a given type of food is proportional to its
fraction in the actual ration. The mean daily rations (C) were
calculated by the equation:

C = H + P + R = ■g(P + R), (1.9)

where H is the unassimilated food, P is the production, R is the rate of
metabolism, U is the efficiency of assimilation. The values of R and U
were determined directly in experiments (Shushkina, Vilenkin, 1971;
Shushkina, Pavlova, 1973; Petipa et al., 1971; and others). The mean
daily production was calculated by the equation: P = RKo^l - Ko),
where K2 is the coefficient of assimilated food used up for growth.

The equations related to the functioning of phytoplankton in the
pelagic community were significantly refined, in comparison to the model
of A. A. Lyapunov. An empirical ration was established (Voytov,
Kopelevich, 1971) between the concentration of phytoplankton and
detritus in the water and the light attenuation factor, which makes
equation (1.2) more concrete:

a = 0.01 + 0.001(p + d). (1.10)

According to Ryther (1956), the variation in the intensity of
photosynthesis with light flux I can be expressed as follows:

(I ^ )
P'n = Pmax^r-^ "^ , (l.H)

p " f^max"

opt

where Iqp^ is the light flux at which the maximum photosynthesis P^,^^ is
achieved. This relationship can be replaced by the following equation,
which is closer to the empirical data:

326

Pp = P'p(l - lOO.l nN)0.6, (1.12)

and has the same sense as the Michael is-Menten equation.

In addition to limitations as to light and concentration of
nutrients, the limitation of production of phytoplankton resulting from
the maximum breeding rate was also considered.

In describing the hydrological situation, a three-layer model was
used. In the surface layer (0 < z < z-,), high coefficients of turbulent
diffusion were assumed: in the pycnoctine (z^ < z < z^) the coefficient
of turbulent diffusion decreased rapidly, and only at greater depths (z
> z^) did the intensity of mixing increase once more. The values of z^
and Zo, defining the depth and thickness of the discontinuity layer are
assumed in the model to be dependent on the time of development of the
ecosystem (see Fig. 3).

The rate of natural descent of the phytoplankton (co, ), bacteria
(a)„) and detritus (w_) are assumed to depend on the density of the
water, which is determined by the vertical distribution of temperature
and salinity.

Vertical migrations of a part of the zooplankton were simulated in
the model so that the food requirements of the elements (f4, Sj^, Sp, S3)
inhabiting the 0-50 m layer are supplemented by a certain portion (K™)
of the total food requirements of the same elements located in the 50-
150 m layer.

A schematic diagram of one cell of the model is shown in Figure 2,
its spatial arrangement--in Figure 3. A water column was considered,
extending from the surface to a depth of 200 m and divided into 20
elementary 10-meter cells. The relationship between cells located
vertically one above the other was determined by the penetration of
light (a), turbulent diffusion (k), sinking rate of phytoplankton (w )
and of detritus (w^). The daily input of light energy from the surface
of the ocean (Iq) and the concentration of nutrients at 200 m depth
(C2qq) were assumed constant.

The horizontal displacement of the column of water was assumed to
occur under the influence of a constant current with uniform
distribution of velocity with depth. Vertical transfer of the water was
by turbulent diffusion.

Under these assumptions, it becomes possible to replace the
horizontal displacement of the water column containing the simulated
ecosystem being modelled with the time of existence of the ecosystem
from a certain initial state. In our case the initial state
corresponded to the moment of ascent of the deep waters in the upwelling
area.

It was assumed that in the initial state (t = 0) , all elements of
the simulated system were evenly distributed with respect to depth. The
study of the model showed little sensitivity of the system to the

327

y///MM^/M^)m>{^////^^^^^

Fig. 2. Schematic diagram of a cell of the model considering the distribution
of the elements of a pelagic ecosystem: J--solar radiation; P--biomass of
phytoplankton; Pp--production of phytoplankton; n--concentration of nutrients;
b--biomass of protozoa; f2--biomass of microzooplankton; f3--biomass of fine
filter feeders; f4--biomass of coarse filter feeders; si--biomass of cyclopoids;
S2--biomass of carnivorous calanoids; S3--biomass of chaetognaths and polychaetes.
DOM--dissol ved organic matter. Remaining symbols same as in Figure 1.

zoo

Days

Fig. 3. Placement of cells of model simulating the vertical distribution of
elements (horizontal shading marks area of pycnocline): symbols in circle same
as in Figure 1.

328

selection of initial values of the biomass of the elements.
The system of equations of the model is as follows:

41= - al (1.13)

dz

f = - hPp * «d * n I R, . K |j . 6 |1

i = p]^,b]^,f ...f4, S;^...S4 (1.14)

dz'

^ = aPp - Rp - pp - 1 Cpi + K — I - 0)1 ^

i - f ]^ . . .f^

1^ = Pb - Rb - Pb ■

•iClJ*K0-

8b
"2 8z

j = f j^ . . .f^

3Xi

- iii X-; - > C-i -i

(1.15)

(1.16)

j = P]^,b]^,d^,fi. ..f4,S]^,S2 j = f2...^4» S1...S3 (1.17)

^ = 1 (Hi + wiXi) - ). Cdi + K -^ - 0)3 ^

i = fi...fi,Si...S3 i = fi...f4, (1.18)

where ri is the coefficient of nutrient release in the process of
metabolism, as a fraction of the utilization of nutrients in metabolism
(n = 0.05); C^ ^ is the specific ration of the ith food consumer
represented by the jth food source; u is the natural mortality
coefficient; X^ is the biomass of the ith zooplankton element (i = f^,
^2' ^3» ^4' ^1» ^2> ^3)' ^i is the nonassimilated food of the ith
zooplankton element.

H. = (1 - u^) I Cji
j = p, b, d, f, s.

The remaining symbols are explained above or are analogous to the
symbols used in the model of A. A. Lyapunov (equations 1.2-1.7).

329

The system of equations of the model was reduced to a finite-
difference plan with a time step of one day, a depth step of 10 m.

Figure 4 shows the change in biomass of elements of this system
with the passage of time and, consequently, increasing distance from the
zone of the water ascent. The biomass of phytoplankton and bacteria
increased most rapidly. The fine filter feeders lagged somewhat in
their development, coarse filter feeders developed still more slowly,
their biomass reaching its maximum only on day 30 of existence of the
system. Nevertheless, their combined effect on phytoplankton and
bacterial plankton, in addition to the retarded growth of the bacterial
plankton due to exhausting the reserves of biogens, leads to a sharp
decrease in the biomass of phytoplankton and bacterial plankton. The
inertia of the predators is still greater than that of the filter
feeders: the biomass of the various groups of predators reaches its
maximum only on day 35-50 of existence of the community.

On day 50-60, the system reaches a state which is near steady. It
is characterized by low biomass of living elements and balance between
production and consumption of phytoplankton. This mature state of the
community typically shows little variability of the elements with
further passage of time and, consequently, little variability in space,
and is the state observed in oligotrophic water areas in the tropical
regions of the ocean, particularly the halistatic zones of the planetary
convergences.

The model data agree qualitatively quite well with data obtained by
observation in the ocean. A comparison of the values of biomass of the
elements of the ecosystem obtained from the model with those observed in
the field is presented in Table 1. Considering the relative coarseness
of the model, its agreement with the original can be considered
acceptable.

The model changes in vertical distribution of the elements of the
ecosystem with time are presented in Figure 5. During the early period
(t = 5 days), when the total quantity of phytoplankton was almost
maximal, its biomass was evenly high in the 10-50 m layer. All the
other living elements of the ecosystem have a more or less sharply
expressed maximum, related to the thermocline. However, by the 10th day
the reserve of nutrients in the upper layer was almost completely
exhausted, while at a depth of 10-20 m the maximum biomass of the
phytoplankton was still retained. Deeper, at the upper boundary of the
thermocline, nutrients passing through the thermocline began to form a
second, lower, maximum, which was still poorly expressed. This dual-
maximum structure is characteristic for the vertical distribution of
almost all elements of the ecosystem (Vinogradov et al., 1971).

As the stock of nutrients in the surface layer decreased, the
vertical transfer of nutrients from beneath the discontinuity layer
continued to play an increasingly significant role in the functioning of
the ecosystem. The lower maximum of biomass of phytoplankton became
greater than the upper maximum. As the thermocline continued to descend
to 80-100 m and deeper, the illumination at its upper boundary became

330

, tZDO

Fig. 4. Change of total biomass of living elements of a pelagic
ecosystem from the tropical regions of the ocean in the 0-150 m layer:
P--phytoplankton; f^--Protozoa; b--bacterioplankton; ^2."
microzooplankton; f3, f/i--fine and coarse herbivores; Sj--Cyclopoida;
S2--carnivorous Calanoiaa; S3--Chaetognatha and Polychaeta.

insufficient for intensive development of phytoplankton. A situation
was created in which the lower maximum "separated" from the thermocline,
and its position was subsequently determined by the lower limit of
illumination and the flow of nutrients from deeper levels.

With still more mature state of the community (over 60-80 days), in
the oligotrophic and ultraoligotrophic regions, according to the model,
almost complete disappearance of the upper maximum of all elements
should occur. Actually, the upper maximum disappears only for the
phytoplankton, continuing to exist for the zooplankton even in
oligotrophic regions. An analogous picture is yielded by several
modernized versions of this r-.odel (Vinogradov et al., 1975).

The results produced show that many of the existing features of
vertical and time distribution of elements in the pelagic ecosystem of
the tropical regions of the ocean can be quantitatively reproduced and
explained by means of the model described. However, many important
aspects of the functioning of pelagic ecosystems still remain outside
the model. The assumption of constancy of the velocity vector of a
current in the 0-200 m layer and resulting absence of horizontal
displacements hardly agrees with the picture actually observed in the
ocean. Finally, the model developed fails to consider the final trophic

331

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332

0 /SJO'/S d

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1—1 — r

Fig. 5. Changes in vertical distribution of elements of an ecosystem for
moments in time (t = 5 (1), 10 (2), 20 (3), 30 (4), 40 (5), and 60 (5) days)
vertical line shows depth, m. Horizontal dotted line shows upper boundary
of thermocline; n = nutrients, other symbols same as in Figure 4. Note
the difference in scales used for the different elements.

333

links in the chain--fish, cephalopods, and aquatic mammals, which are of
the greatest interest from the standpoint of their utilization.

Let us analyze some other approaches to the construction of
simulation models of pelagic ecosystems.

1.3. Model Considering the Distribution of Elements by Area

The modelling of changes in the pelagic ecosystem not in depth, as
was done in the previous section, but rather over the area of a body of
water, can serve as another approximation of reality. This approach is
particularly important for water areas with a complex system of surface
currents and various faunistic groups in the plankton.

The prototype for the creation of a model considering the
distribution of elements over a water area (Menshutkin et al . , 1974) was
the Sea of Japan, in which, due to the sparsity of shallow zones, we can
separate the open part of the sea as an independent pelagic ecosystem.
The strong but inconstant flow of water through Tsushima Strait creates
significant horizontal heterogeneities, justifying the model type
selected. In addition to the passive transfer of hydrobionts with the
current, nektonic animals actively migrate through Tsushima Strait--
squid and fish--entering the Sea of Japan in the spring and summer and
leaving it in the winter.

To make the model more concrete, ecologic-faunistic characteristics
of the plankton of the Sea of Japan and data on the trophic
relationships among the primary groups of its population, obtained
during the 52nd cruise of the VITYAZ' and a number of shoreline
expeditions, were used (Pasternak, Sushkina, 1973; Sushkina, 1972).

In constructing the model, the entire water area of the sea was
divided into squares 150 km on a side. Each square corresponds to an
elementary cell of the ecosystem, in which the volume of water down to a
depth of 200 m is studied. Within each cell, the heterogeneities of
horizontal distribution of abiotic and biotic elements are assumed to be
insignificant.

The transfer of dissolved matter or suspended particles of
detritus, phytoplankton and zooplankton from one cell into another
results from the currents. A diagram of the currents presented by I. V.
Sizova (1961) was accepted, with the loss of detail resulting from the
size of the cells. Seasonal changes in the speed of the Tsushima
Current, following S. Nishimura (1969), were considered sinusoidal with
a maximum in September. The effective temperature (mean water
temperature at which the population of a given species finds itself in a
given cell) was assumed to be a function of time and the coordinates of
the cell, while the temperature field was taken from S. Nishimura
(1969).

Each cell of the model of the ecosystem contained twelve elements
(Fig. 6). The group of inanimate elements was represented by the
concentrations of nutrients (n) and detritus (d). Plankton was divided

334

^y//////////////////////////////////^^^^^

Fig. 6. Schematic diagram of a cell of the pelagic ecosystem of the Sea
of Japan: jQ--solar radiation; n--nutrient concentration; p--
phytoplankton; b--bacterioplankton; d--detritus; f^--boreal herbivorous

f3--interzonal

epiplankton; f2--warm-water herbivorous epiplankton;
herbivorous zooplankton; Sp-carnivores of the boreal complex; so--
carnivores of the warm-water complex; qi--fish; q2--squid; 6 — water
temperature; W--transport by currents; Y--catching of fish and squid,

w'„, w"^--seasonal vertical

oj^--active migrations of fish and squid;
migrations of interzonal plankton.

2'

into three groups of organisms: microplankton, mesoplankton I
(herbivores) and mesoplankton II (carnivores and omnivores). The
composition of the microplankton included phytoplankton (p) and
bacterioplankton (b). Mesoplankton I included boreal epiplankton f^,
warm-water epiplankton ^2. ^nd interzonal plankton f3. The seasonal
vertical migrations of interzonal herbivores were considered, and a
special element was distinguished--the wintering stock (f '3)--interzonal
zooplankton which spends the winter at depths greater than 200 m. It
was assumed that the wintering stock is not moved by the surface system
of currents. Two elements were distinguished among the mesoplanktonic
carnivores and omnivores: species of the boreal comples (sj^) and
species- of the warm-water complex (S2)-

In contrast to the planktonic elements, passively transported from
cell to cell by currents, the elements of the nekton (fish--qi and
squidS'-qp) can move actively. For lack of a better hypothesis, it was
assumed that the fish and squids search out the maximum of food in the
cell in which they are located in neighboring cells. The rate of

335

movement of fish was assumed to be 10 km/day, of squids 15 km/day.

One peculiarity of the model in question is that the elements of
the cells of the ecosystem are combined into groups. A group includes
elements with similar dimensions of individuals, type and spectrum of
feeding, and interaction with predators. Essentially, the organisms
combined into a group occupy a single, broad ecologic niche. However,
the reaction to abiotic factors, energy characteristics and
peculiarities of migration remain specific for each such element. This
separation of trophic groups greatly simplifies the modelling algorithm
and does contradict the biologic essence of the process being
modelled. The time step of functioning of the model was 5 days.

Operation of the model began with an arbitrary initial state,
assuming even distribution of all elements of the ecosystem over the
water area of the sea. After three years, functioning of the model led
to a state which was near steady, in which the difference in the states
of the elements of the ecosystem for any given date of any two years did
not exceed 10%.

The data, averaged over the entire surface of the Sea of Japan, on
monthly production of phytoplankton and zooplankton, bacteria and nekton
show that the production of phytoplankton has two rather sharp maxima.
The mean annual production of phytoplankton of the entire Sea of Japan,
according to the model, is 1,280 kcal/m^ per year--a quantity which is
quite probable, judging from the data of Yu. I. Sorokin and 0. I.
Koblentz-Mishke (1958). It is difficult to evaluate the likelihood of
the values of production of bacterioplankton and zooplankton obtained in
the model due to the lack of field determinations. The production of
the higher trophic levels (commercial fish and squid) can be compared
with their catch levels (Moiseyev, 1969). According to the model, the
annual fish catch (30% of the ichthiomass present), with a calorie
content of 1 kcal/g of wet mass, would be 820,000 tons for the entire
Sea of Japan, of squid--540,000 tons. The actual fish and squid catch
is about 1,000,000 tons, the potential possible catch--about 1.23
million tons (Gulland, 1970).

The distribution of biomass of phytoplankton over the water area of
the Sea of Japan, according to the model data, is shown in Figure 7. In
the winter there are only small accumulations of phytoplankton along the
coast of Japan in the region of the Noto Peninsula and further south.
Intensive vernal development of phytoplankton occurs in Petr Velikiy Bay
and the entire central portion of the sea. By summer, the area covered
by accumulations of phytoplankton is reduced and is divided into two
areas--along the coast of Japan and Primor'ye. In the fall, the eastern
and central portion of the sea contains high phytoplankton biomass.

Boreal epiplankton in the uper 200 meter layer is quite sparse
during the winter months. In the spring (March) the water area of high
concentration is significantly expanded and in the summer (July), the
area with a biomass of over 1 kcal/m^ covers almost all of the
northeastern portion of the sea, including Petr Velikiy Bay.

336

Fig. 7. Model maps of the distribution of certain elements of the ecosystem
of the pelagic zone of the Sea of Japan: P, phytoplankton; f3, interzonal
herbivores; f2, herbivorous and omnivorous zooplankton (southern forms);
q, nekton (fish and squid); 1, biomass kcal/m^; 1, > 10; 2, 10-5; 3, 5-1; 4, 1-
0.1. Points represent centers of cells of the model.

337

Interzonal herbivores, which make up the main mass of the summer
plankton, are rather evenly distributed in the winter over depths of
more than 200 m throughout the entire cold-water portion of the sea. In
the spring, they migrate to the surface layer, where their biomass
rapidly increases, and in the summer, over most of the water area, their
biomass is at least 5 kcal/m^ (Fig. 7). The seasonal dynamics of the
spatial distribution of the boreal omnivorous mesoplankton, in its most
general features, repeats the distribution of interzonal herbivores, but
with significantly lower biomass.

The distribution of southern forms of zooplankton (Fig. 7) is
determined basically by the temperature conditions and mode of the
Tsushima Current. In winter, their main mass is concentrated along the
coast of Japan. In spring, heating begins and the arrival of warm water
and zooplankton from Tsushima Strait increases, reaching its maximum in
fall. As a result, during the fall the area of distribution of the
southern forms of zooplankton covers almost the entire southeastern
portion of the sea.

The migration of nektonic animals (fish and squid) begins in the
spring in the southern portion of the Sea of Japan and follows 2 main
tracks: the more numerous stream is directed along the Honshu coast to
the northeast, the less numerous stream--along the coasts of Korea
toward Petr Velikiy Bay. In the summer and fall, significant numbers of
squid, according to the data from the model, are observed in the central
portion of the sea in the zone of contact between the Primorskiy and
Tsushima Currents (Fig. 7).

Unfortunately, there are no sufficiently complete data available on
the true distribution of the biomass of phytoplankton, bacterioplankton
and zooplankton, fish and squid in the water area of the Sea of Japan in
the seasonal aspect. Therefore, the question of the degree of accuracy
of the model which has been created remains open, although we can note
that the picture of distribution of zooplankton obtained in the model is
not contradicted by the available (though rather fragmentary)
observations of the distribution of its biomass. The distribution of
squid also agrees in general terms with the observed distribution
(Zuyev, Nesis, 1971).

The model in question shows the actual possibility of quantitative
description of the seasonal changes and distribution over a water area
of elements of a pelagic ecosystem. Obviously, models of this type can
yield not only production, but also zoogeographic information. The
separation of species of boreal and warm-water complexes in the model of
the Sea of Japan is a step in this direction.

It must be considered that models of this type are quite sensitive
to the quality of hydrologic data used. The need not only for a general
diagram of currents, but also for values of mass transfer in each square
of the water area, as well as precise values of the coefficient of
horizontal turbulent diffusion, places certain limitations on the area
of application of such models.

338

1.4 Model Simulating the Volumetric Distribution of Elements

The transition to three-dimensional models is a natural development
of the models discussed above. This transition is particularly
necessary upon analysis of upwelling zones or areas of the ocean with
strong subsurface countercurrents. Let us study the ecosystem of the
eastern portion of the equatorial Pacific, where we encounter a complex
and unique structure of the field of currents. To represent the
situation which has developed there as a plane model would be an
unjustified simplification. On the other hand, v/e do not have
sufficiently complete information concerning the field of currents and
coefficients of turbulent diffusion in this region of the ocean.
Therefore, we must, for now limit ourselves to a very simplified,
approximate plan, which is more qualitative than quantitative in nature.

Figure 8 shows a block diagram of an elementary cell of the model
and the location of the cells in space. Keeping in mind the qualitative
nature of the model, the structure of the trophic network of a cell has
been greatly simplified and includes nutrient salts (n), detritus (d),
phytoplankton (P), bacterioplankton (b), herbivores (f), and carnivores
(s).

XM f

Fig. 8. Block diagram of 3-dimensional model of pelagic ecosystem and
3-dimensional placement of cells of the model. Arrows show transfer by
currents. In the box, we show the relationship between concentration of
nutrient salts (n), phytoplankton (P), bacterioplankton (d), detritus
(d), herbivores (f), and carnivores (s).

339

In all, there are 216 elementary cells in the model, forming a
parallelepiped, extended along the equator. The distance between the
centers of cells in longitude (X axis) is 1,000 km, in latitude (Y
axis)--100 km, in depth (Z axis)--40 m. The system of currents was
selected so as to imitate the surface trade current (along the X axis
from the coordinate origin) and the Cromwell current, gradually
approaching the surface (directed parallel to the X axis, but toward the
coordinate origin). In the immediate vicinity of the equator (plane
XZ), there is a significant vertical component to the velocity of the
flow, leading to ascent of waters to the surface.

The surface current, directed toward the coordinate origin and
flowing parallel to the X axis some 500-600 km to the north of the
equator, imitates the equatorial countercurrent, in the area of which we
find the convergence zone. The model imitates the outflow of surface
waters away from the equator (movement along the Y axis from the
coordinate origin) and the corresponding deep countercurrent (parallel
to the Y axis toward the coordinate origin). The maximum vertical
component of speed of the flow is equal to 5 m/day (0.6 -lO"^ m/s), while
the maximum horizontal speed is 50 km/day. The diagram of the currents
was selected so that the condition of continuity is maintained for each
cell. The model considers the transfer of elements of the currents and
the gravitational precipitation of detritus.

The initial state of the model was assigned in the form of an even
distribution of all elements throughout the entire volume analyzed.
After 30-40 days of the transient process, the model approached a stable
state, in which the flow of biogenic salts toward the bottom surface of
the parallelepiped was balanced by precipitation of detritus through
this surface.

The maximum concentration of phytoplankton is created in the area
of the maximum intensity of upwelling (coordinate origin). As we move
along the X axis (along the equator toward the west), the concentration
of phytoplankton decreases, while the maximum itself descends to a depth
of 80 m. This result agrees both with observations at sea, and with
data obtained in a 2-dimensional model.

The distribution of biomass of herbivores is characterized by the
formation of two areas of concentration: one is located on the equator
to the west of the region of intensive upwelling, while the second is
extended in the latitudinal direction north of the equator in the
convergence zone. It is characteristic that the maximum concentration
of phytophages is deeper in the zone of the convergence.

The area of predominance of carnivores is extended in a broad strip
from east to west in the zone of the northern trade current. The
maximum concentration of predaceous zooplankton is found at a depth of
60-120 m. In the stable state of the model, the carnivores are
distributed almost throughout the entire volume down to a depth of 200
m, which is less typical of herbivores and not at all typical of
phytoplankton.

340

A comparison of the distribution of elements of the model with
observed data in the equatorial portion of the east Pacific (Vinogradov,
Voronina, 1963; Voronina, 1964; Blackburn et al . , 1970) shows
qualitative agreement of the distribution of phyto- and zooplankton in
the model and in the field. The decrease in the concentration of
phytoplankton to the west as we move along the equator appeared rather
clearly in the model, in spite of its approximate nature. The maximum
of predaceous zooplankton in the area of the convergence at 5°N is also
noted in the model although another maximum of carnivores, on the
equator between 150 and 160°W, is almost not reflected in the model. It
is possible that this is related to the elevated values of horizontal
flow speeds in the model, or to the fact that only predators with
characteristic dimensions of not over 10 mm were analyzed.

This model, despite its extreme sketchiness and the qualitative
nature of results produced, demonstrates the genuine possibility of
creating 3-dimensional models of pelagic ecosystems in the ocean.
However, the experience of development of models of this type has shown
that there are significant difficulties. First of all, clarification of
the 3-dimensional field of the velocity vector of a current, even for
steady conditions, is a complex, cumbersome and, at the present time,
sometimes impossible hydrophysical task. Secondly, to ignore processes
of turbulent transfer, as this model does, is possible only as a first
approximation. Consideration of horizontal and vertical turbulent
transfer, however, would introduce new complications. In 3-dimensional
models, consideration of the active movements of zooplankton and,
particularly nekton, becomes extremely necessary, greatly complicating
them in comparison to 1-dimensional and plane models.

341

2. Stochastic Models of Communities. (B. S. Fleishman)

A community is a complex open stochastic system (Fleishman, 1976),
but its deterministic models are justified in the first approximation by
the law of large numbers.

There is an extensive literature on deterministic dynamic models of
community, based on differential, finite-difference and matrix
equations.

A community consists of components--populations or groups of
populations, distinguished according to some principle. The individuals
of component a, in turn, may form a stable formation of n^
individuals. This formation will be called an a-individual . Their
number in a certain biotope of volume V will be represented by H^. The
density of the a-individuals (density of the biomass) will be denoted by
the expression p^ = N^/V (B^ = Pa^a). where 6^ = "a^a is the mean
biomass of an a-individual, B^ is the mean biomass of an individual of
the a-component.

Theoretically, we can divide a biotope of volume V into N
elementary cells of volume aV, occupied by only one a-individual or
empty. Suppose V^ = aVN^^ is the volume occupied by a-individuals, while
^a+l ~ '^VNa+i is an empty volume with N^+i elementary cells

( Z N« = N).
a=l

If we analyze a stochastic model of a community without considering
the aggregation of a-individuals, i.e., if we consider all placements of
the Nc( a-individuals in the N cells equally possible, then the
probability of presence of an a-individual in any cell (probability of
an a-individual) is equal to p^ = HJH, while the probability of an
empty cell is equal to Pa+i = Ng+i/N. It is easy to show that the
probabilities are proportional to the densities p^ = PqAV. However, the
introduction of probabilities is important, due to the possibility of
working with them and using the apparatus of the theory of
probabilities.

Thus, the status of a community is described by a probabilistic
vector p = (pc(). If the ath component of the community consists of one
population, it can be divided into b^, age groups, considering p^ - (p^s)
to be a vector, where p^^s is the probability of a-individuals of the sth
age group.

342

2 .1 Dynamic Model of a Community Ignoring Aggregation

The succession of a community (Odum, 1975) can be described by a
stochastic model with discrete time t = 1,2,.... The time step taken as
unity corresponds to the characteristic time interval for the community
in question: a day, a month, a year. The status of the community at
moment in time t+lp^"''-'- in the model in question can be represented as
fol lows:

pt+1 = ptPt, (2.1)

where Pt = ||P^3|| ( »» 3 = l,a)--is a stochastic matrix. In order to
consider the effect of delay in the reaction of the community, we can
require that the probabilities p^ag depend on the k states p^'l*^ , . . .p^-l ,
preceeding state t.

pW = pW(p^-^---.P^-M or Pt = Pt(pt-k,....pt-l). (2.2)

The specifics of each community, related to the trophic and
tropical structure of interactions of its components, as well as its
interaction with the environment, is described by the unsteady equations
(2.2). Recording of these data, together with the k first states
p ,...,p , unambiguously defines all subsequent states of the
community. However, certain modifications of these interactions are
always possible, which ecologists consider permissible within a given
community (not leading, from their point of view, to a new community).
In our model, this is formalized by the assignment of a certain set Wg
of permissible functional transforms (2.2), describing the very same
community.

A climax community (Odum, 1975) corresponds to the limiting
behavior of the model as t->". The limiting state p = lyn pt exists if
there is a limit P (.,...,.) = li^ Pt( .,...,.) , corresponding to steady
influence of the environment and relationships within the community in
the climax state. The limiting state is independent of the k initial
states and can be found from the equation

p = pP(p,...,p) (2.3)

It is convenient to find the solution of this equation in two
stages. In the first stage, we seek out the solution of the linear,
homogeneous equation p = p||pag|| to express p through p^g

P = FLp^g] (2.4)

343

In the second stage, we solve the transcendental equation
P = F[p.T^.{p,...,p)]

(2.5:

for p. In accordance with what we said above, the community at climax
corresponds to the set U={iipc(3ii} of limiting values, corresponding to
the permissible set Wg={pc(3( .,...,.) ^ of the functional transforms
Pu3( .,...,.) . We note that a portion of the functions p^^p^l .,...,. ) may
be independent of p.

Let us analyze an explicit solution of the equations presented for
the model of the community, based on the characteristics of birth and
death of a-indi viduals . These characteristics, as resultant indices of
interactions of the components of the community among themselves and
with the environment, are widely used, primarily for the description of
the higher trophic levels of community.

Let us introduce the conditional probability of birth
conditional probability ii^ of death of an ct-indi vidual of
corresponding age in one time step.

It can then be shown that :

4s '
the

and the

/ Pn

^'= 0

0

pUi \

Paa + l

"aa Paa+l

.Pa*n ■ ■ ■ Pa.ia ■ ■ ■ Pa^^a Pa^t.a^x
pLxa - (K, 0, ■ . ., 0). p^^,^^^^ = 1 - i A^

P'aa

0

^aba-l Kba,-l^'ah^-i

(2.6)

~^'„

"''a-l

f'ah„

344

'as

Equation (2.4) in this case has a simple solution:
\ ^ \ ^ Q* h P

n„ , "^^ P

ofl. Pofl = U V'l s='r PTJ" • (2.7)

^ul+i^al u=2 X^u+^^au "^' ^' ' «=1 s=l Pa+i

complete solution of system (2.7) requires explicit assignment of the
variation of X^ , xt^ and u^ with p^ and the parameters of the
environment. In addition to the variations which are specific for each
community, at least the following two are common. Suppose the
conditional probabilities X\ of birth of cx-indi viduals of the first age
group from a-indi viduals of age groups (probabilities of fertility by
ages) are assigned.

Then :

xt =

;|J' >^IpIs • (2.8)

On the other hand, suppose the death of a-indi viduals , defined by
the probability u^g , depends on K independent events--both in the
environment and within the biocenosis (catastrophies , fishing,
predators, parasites, food shortages, natural death, etc.). The
probability of these fatal events is represented as M^gi^ (k=l,K) . Some
of them, in turn, may depend on the status of the system p'-.

Then, as we can easily demonstrate:

mIs = n + [^1^ (p'ik - 1)'^]"^}"^ . (2.9)

We note that only where Pctsk^c<l does approximate additiveness
occur:

K

v\s = kli i^ask + 0 (c) , (2.10)

which, as a rule, is not considered in the ecologic literature.

Let us study a few particular cases of the relationships we have
derived. Let us begin with the case of a single population (a=l),
divided into b-^ age groups. Using equations (2.1) and (2.6) in our
case, we produce, for the probability of the first age group

t+1 t t t t t
p = p (1 - y - X ) + p X . (2.11)

11 11 11 11 2 1

We will consider that the reproductive capacity is equal only for
age groups beginning with group Sq. Mathematically, this can be
expressed as:

345

,0

for 0<s<Sq -1

^ = {
1 f

for SQ'.s<b^

(2.12)

Furthermore, we will assume the quantity f, which characterizes
this reproductive capacity, to be a function of the summary probability

h=

^1

I

s=s

0

Is

of the reproductive age groups. Then, equation (2.11), considering
(2.8) and 2.12), can be rewritten as:

^t+1 = V(St).

where

^t+1

{p

t+1
11

t t

p (1-P
^11 11

t t

has the sense of "supplementation," while S^ has the sense of a

of this ■

reserve. Recurrent equations
literature without a probabilistic
using a deterministic matrix model
Stocks and Recruitment (1970); for
available, while for f (S)=( aS+B)-l

type are widely used in the
basis. A basis is developed for them
developed by Lesley in the book Fish
f (S) = aexp(-BS), a Ricker model i"s
the model of Beverton and Holt can be

used, or a and p are constants (Beverton, Holt, 1957).

The remainder of our brief presentation concerns the case of an a-
component community (a>l) with components not divided into age groups
(bc(=l). Representing ycti = Uct and Pal=Pcx. using equation (2.7) for the
steady case, we obtained:

g

Pa ~ p Pct+l '

a

a X

a=l a

a,-l

(2.13)

For the remainder of our presentation, the particular case of
equation (2.9) when K=2 is important:

X +y -2x V
y^ = m(x^, y J = 1 „ ., (a = 1, a).

TTx

or a

(2.14)

where x^ and y^ are the probabilities of death of an a-individual due to
causes inside and outside the community, respectively.

346

2 .2 Model Study of Optimal Strategies of a Community.

The structure of a community in our model is defined by the vector
x-(Xfy) of the death of an a-individual from causes within the community,
particularly natural death related to the trophic structure, etc.
Obviously, it is less variable with time than is the vector X = (Xot) of
birth of a-individuals. Therefore, vector x will be considered a fixed
parameter of the model while vector x, defining the behavior of the
community, will be considered variable.

As an indication of the limiting effect of the medium on the
community, we can report the mean value X*, while we can use the mean
value y of the mortality vector y=(ya) due to extrabiocenotic causes
(behavior of the environment) as an indicator of the intensity of the
action of death-causing factors of the environment on the community.
The set of vectors y and X, with nonnegative components, not exceeding
unity, with fixed values of y and X, will be represented
by W- and W- . Furthermore, additional conditions are placed on
vect'^r X, related to equation (2.2). Therefore, the set W^ of its
possible values is included in the set W-(W^ W-) . We note that
analogous limitations on the vector p=(Ma) ^" ^^^ case extend only to
the fixed vector x and do not effect the vector y.

Empirical analysis of succession processes in a community reveals a
tendency toward S- shaped growth of its summary biomass right up to the
limiting climax value, limited by the steady conditions of the
environment. This tendency, accompanied by fluctuations in the biomass
of the individual components, is considered by Yu. Odum as a strategy of
the community (Odum, 1975, p. 345).

Let us formalize these general ecologic concepts within the
framework of the model for quantitative analysis which we have studied.

Grouping populations within components, we can achieve relatively
small differences in mean densities 3a of the biomasses of a-
individuals. If this, for any reason, cannot be done, then we must
limit ourselves to analysis of only the higher trophic levels of
multi component communities, for which B^ is not divided into orders.
The assumptions we have made allow us to extend the tendency toward
growth of the summary (or mean) biomass of the community to the mean
population density p, which is proportional to the mean
probability p (see above). Thus, we can consider the following
function, monotonically increasing p, to be the "goal funct onal" of the
community:

M = M(X,p) = p/X(l - ap) = J^ E WWa=i(-)- (2-15)

Xci a=l XV

la
*In what follows, the averaging operator x represents x= — S-iXq

see (2.13) . " ""^

347

The strategy of the community is to maximize the value of M
(max M ) with respect to XeW^ .

^ y

There is no basis for advance determination of the degree of
indifference of the environment to a community, therefore, in order to
guarantee the following results and conclusions, we must expect the
"worst" action of the environment on the communit^^ y, i.e., that action
which would minimize M['^''"y^J with respect to yeW^. Thus, we must
analyze the expressions: ^

min max M [x, y(x, y)] < min max M[x, ij(x,y)], (2.16)

yeW- XeWv yeW- XeWv

•^ y X y X

max min M[X, p(x, y)]< max min M[x, u(x,y)]. (2.17)

I

X -^ y X -^ y

^We note that whereas in function M as we expand the set of values
of W— to W- no new maxima appear with respect to x, relationships (2.16)
and if2.17)^are converted to equations. This occurs for all cases of
practical interest.

First of all, let us produce general estimates using the equation
M = M(x, \i ) , by varying X and p. It can be shown, by using the
Bunyakovskiy equation, that:

max min M(X, u) = min max M(X, u) = M(Xe, lie) = — — , (2.18)
X y u X y

where e = (1,...,!^). However, the requirement for constancy of

Pet = M(Xct, ya) - V is unrealistic, if we consider the variability of the

vectors of x and y.

Consideration of the conditional extremes with respect to x and y
involves great analytic difficulties and leads to the following
results. The minimax equation (2.16) leads to a degenerate case of a
community (some of the components of vector X vanish). The maximin
equation (2.17) leads to the following important results.

Let us represent M{x, p(x, y)} = Mx(x, y) and

min(l-y, 1-y) = M (X- y-, X-) =

max M (X, y-, X) = max min M (x, y),

A Jf X

XeW^ XeWy yeW-

348

where y— , A is the extreme value of y with fixed yand X, while X— is the
extreme^ value of x with fixed y and X. ^

Of primary significance is the function:

obtained by replacing in M (X, y- , X)the extreme value of x = x- with

X y^ y^

the extreme value of X = X- (y^^y,). This function, as in the theory

of Statistical selection among hypotheses (Basharinov, Fleishman, 1962)
will be called the operative characteristic. Using the method of
multipliers, we find its expression:

m(z^, z^) = uCx^) + y(x^, X2) "^v'lz^) v'fz^) (z^ - z^), (2.20)
where the function v(Y) is the solution of the transcendental equation:

i = Urr^) + v-1] (2.21)

while the function X(z., z^) is:

y=y(z, ,z.)= \Lll^ I \y^ , (2.22)

^ ^ '''v'(i^) Vv'(I^)

while the expression Vq(z) is defined as follows.

Equation (2.21) has a solution if the structure of the community is
"linear," in which case:

1 - 2x^ a - 1

- = C + A T" ( a = 1 , a) ,

1 - X ^ " ^"^"T

1-2x1 xi-Xa

where C = ^j and the quantity a = ,, „ \/i ^ \ characterizes the

1-xi ^ ^ (l-xi)(l-Xa)

"standardized difference" of mortality of components of the community.

349

for large values of a, we can obtain an explicit expresion for v(z):

v(z) = vA (Y) = [gA"^(z) - gA"\(3;ZZ)]]-l, (2.23)

1 - 2x

where

gA(z) = (e^^ - 1)/A, (2.24)

and, since Qq^z) = "z , then;

vn(z) = [(z)-^ - [(IIZZ))-1]-1. (2.25)

1 - 2x

It is convenient for the remainder of our presentation to introduce
the following function:

v(z,) - v(Zp)
6 = 6(Zp z^) = — . (2.26)

•^v' (z^) v' (Z2) {z^ - f^)

It can be shown that in the linear case, when v(z) = v (z) the
corresponding expressions >^ = A^ and "5 = 6^ become:

(1 + A/C) - e^^l In (1 + A/C) - AZp ,,- -- .,,
YA = L_ . e"^^^r^2' '^ (2.27)

(1 + A/C) - e^^2 In (1 + A/C) - Az^

and

, = [eA(-Zi-Z2)'2 - e-A(zi-Z2)'2j/,( ) . Shl^U,-Z2)/2l ^

^ ^ A(zi-r2)/2

In general, the extreme values of the conditional probability

^yi.A = (ya^» yyi,Xy2= ^^a^' ^^^ = ^^S^ ^"^ ^'^^ absolute probability
p = (p°) are:

350

whert

yl = ^"i - (A'„ - A-) - (A- + yi)

0 -1 0 ."

Pa = Pf^a!f^,

^a ' 1 - 2x

(l+A-)/X
1 + A- + ,, (L)

1 + .V

1 + A' + r(z,)

( a = 1 , a) .

(-V + y-^

(2.29>

Their analysis, in contrast to the minimax case, produces no
disagreement with general ecologic concepts. For example, dominance
(nonuniformity of density p^ or probability p^) is a result of non-
uniformity of distribution of components of vector A which, in turn, is
a result of heterogeneity of the structured vector x = (x^). If this
vector is homogeneous (^a = ^> ^q " "^0 n ^^ ' ^^(\ characteristics of the
community become homogeneous (y^ = y, x^ e i, pO 5 p ) , In this case,
there are no degenerate values of the components of the vector
A = (a ). Thus, the model in question provides no basis for rejecting
maximifi' optimization of the community. The problem of the sequence of
occupation of the conditional extremes '^'(^ "'I" M or "^i" ^^^ M is of
basic significance. It is related to the fact that tne first case
corresponds to the homeostatic principle of the "stimulus-reaction"
decision, while the second case corresponds to a more complex "reaction-
stimulus" decision, involving prospective activation. Here, in contrast
to the case of populations, at the level of qualitative analysis of the
model, without using empirical material, we must give preference to the
hypothesis that the community follows the principle of "stimulus-
reaction." This indicates some regression of the biocenosis in
comparison to populations, in which pre-adaptation-type "reaction-
stimulus" decisions are quite likely (Fleishman, 1971). These
relationships are of more than qualitative interest. As will be shown
below, they can be used for quantitative analysis of the adaptation
cycle of a community, related to its peak stability (Odum, 1975, p.
347).

In the environment, if there are no anthropogenic factors present,
great deviations are improbable, i.e., large values of y > x are
improbable, and therefore occur rarely (are separated by long mean
intervals of time). During these time intervals, the community succeeds
in adjusting to a state close to the steady state. This means that we
are justified in analyzing only the steady state of the goal functional
(2.15). However, the concept of the norm and the depressed state of a
community cannot be related to any specific value of harmful effects of
the environment y. Furthermore, any such effects, if they have
sufficiently long-term stability, after the community adapts to them
(^ = \}), can be considered normal, and the community itself can be
considered to be in the normal state. This might be called adaptive
accumulation of the harmful environmental effects by the community. In

351

the model we are analyzing, this corresponds to the following formal
identity:

m(x„, y„) H y{p(x^, yj, 0}.

Let us perform the following mental experiment, utilizing the
operational characteristic. Suppose a long-term adaptation, reflected
by vector Ay, places the community in the normal state, which
corresponds, with assigned structure x, to the value of the operational
characteristic m(l, 1). This is its ideal value. Actually, there are
always certain weak perturbing environmental effects y * 0, but in the
normal state y « x we can ignore them, since in this case
m(l - y, 1 - y) - m(l, 1) . Suppose the environment suddenly applies a
strong harmful y > R to the community. In the worst version of this
case, the corresponding value of the operational characteristic will be
m(z, 1), where z=l-y<l-x. Immediately after this, we will
consider the community to be in a depressed state. Then, after a
certain, rather long, time interval has passed, due to adaptation,
reflected by the vector x = x^, the first adapted rise of the community
occurs (increase in mean population of individuals). This corresponds
to the value of the operational characteristic m(Z, Z). Suppose now
that the harmful factor of intensity y = I - z is relieved. Immediately
after this, a passive rise of the biocenosis occurs (increase in mean
population of its individuals). This corresponds to the value of the
operative characteristic m(l, 2). However, this does not exhaust the
capabilities of the community, since over a sufficient period of time,
readapting along vector x from the value x^ to the value Xq, it once
more returns to its previous state, definea by m(l, 1), performing a
second adaptive rise. This sequence of effects and adaptations will be
called the adaptation cycle. In accordance with ecologic concepts, the
corresponding values of the operative characteristic (2.20) satisfy the
equations:

m(l, 1) > m(l, 2) > m(2, 2) > m(2, 1). (2.30)

Their relative difference will be called the first and second

adaptive and passive rises and represented by a^j^, a^2 ^nd a^,

respectively. Their ratios to the maximum value m(l, 1) are represented
by p2 "* 1^3 •* ^^4' i^espectively.

The sum of first values is 1, and the values are expressed through
the parameters y and 6 as follows:

= v^

m(l, l)-m(.-, 1) (2,31)

^ ^ m(l, z) — m{z, z)
m(l. l) — m{l, 1)

A„j = 1 — A„j — An.

352

0,0 0,Z 0,i/ 0,6 0,S Y

Fig. 9. Adaptive {h^^ and A-^o) and passive (a^) rises as functions of
coefficients of nonlinearity (6) and heterogeneity ( t) .

Furthermore, the following estimates are valid:

^^3 > ^al' n ^ ^al "^ ^n-

(2.31')

Therefore, it is sufficient to calculate the first two values of

A,i and A^, in order to determine their weight. The nomogram which this

requires is presented in Fig. 9.

It is important to be able to estimate the mean probabilities p
[see (2.15)], corresponding to values of the operative characteristic of
the adaptive cycle P^ > P2 > P3 > P4- Their ratios to pj^

, _ P2 . „ - P3 . _ _ P4

> TT-,

Pi

values of

U2:

n, - —1. are expressed through the corresponding
Pi Pi
U3 and U4 as follows:

H

l-ap^(l-M^-)

> U,-

(i = 2, 3, 4)

(2.32)

Thus, for full calculation of all of the parameters of interest to
us, it is sufficient to be able to calculate the parameters 6 and y,
which, in the general case, requires solution of the cumbersome
transcendental equation (2.21). Also, the linear case v(2) = v^(Z) fits
practically completely in the jrder of accuracy of the initial experi-
mental data on the values of x^ (a = TT^) . Actually, if we number the
components of the community in order of decreasing mortality of their
individuals x^ > X2 > ••• ^ x > ... > x , and then, using the method
of least squares, straighten their function

1 - 2x,

«-

1 - X.

+ A

353

the quantities C* and a* can serve as experimental estimates of the
theoretical parameters

1 - 2xi . xi - x,
C = ^ and A - ^ ^

1 - Xl (1 - Xl)(l - Xg)

For numerical calculations, it is convenient to analyze the asymptotic
case of small values of a, when the expressions (2.27) and (2.28) are
simplified:

l.i ."A l_i .^ _ . 2- - 2

en 2 c ^2 „ 2 A(z. - zj a'^(z, - zy

YA . ^ ^ (1 ^ L_ + 1 2_), (2.33)

1 Azf 1 - A 2 24

i _ 7 i c" " 1 ?

C ^2 2 ^ ^ 2c^

a2(Zi - z„)2

6A . 1 + ^ ^ . (2.34)

24

To estimate the mean probabilities of a-indivi duals of a
community p, we must estimate the mean birth rate l of its individuals,
limited to a great extent by the trophic nature of the area of
distribution. These estimates represent a special problem in
trophodynamics. The importance of the equations presented above for the
relative indices a and tt consists in that they can be calculated without
knowing the values of l, before they are determined. Let us analyze a
numerical example of the use of these equations.

Suppose, within an a-component community (a = 10) with a mean
probability of a-indivi duals within it pi = 0.01 and assigned parameters
C = 0.1 and a = 0.15, there is a commercial population of interest to us
(component a) and we would like to exploit it annually (time step of
model one year) so that the corresponding parameter y^ = 0.4, while
leaving the other components alone (y = y^ = 0-^ =1-2). What, in
this case, is the maximum possible value of the relative mean
probability of a-indivi duals of the community ^2 = P2/Pi» and what is
the possible increase in v^ to the value 113 = Pt/P^, after some rather
long time of readaptation of the community to the new conditions of
stable (with characteristic y) exploitation?

By definition, we have

773 > 0.5 and 1x2 > 0.75,

the quantities 0.5 and 0.75 were defined as follows: first, using C =
0.1 and a = 0.15 and the equations (2.33) and 2.34), we found the values
of X = 0.5 and <5 = 1 , then, using them and Fig. 9, we determined the
values of a^i = 0.5 and Ap = 0.25; then using them and equations
(2.31'), we found the values of the estimates M3 > 0.5 and P2 ^ ^.75 and
then, finally, using them, we found the desired values of the estimates
TT3 and tt2 (see (2.32)).

354

Obviously, similar estimates can be performed to predict the
results of other strong effects, related to pollution, catastrophes and
other harmful influences on a community.

2.3 Static Model of a Community Considering Aggregation.

The construction of a dynamic stochastic model considering
aggregation is quite difficult. Therefore, let us analyze a static case
of this model or a 2-component community (a=2) consisting of a predator
and its prey, referring to the aggregations of the predator as schools,
of the prey as spots.

A set consisting of N objects will be referred to as a N-set. In a
single biotope with the volume V„(q = 2 for area, q = 3 for volume), we
analyze the N-field of food particles and the M-accumulation of
individual predators. The aggregation of food particles is determined
by the v n-spots (N = v.n), the aggregation of the latter by the u m-
schools. Furthermore, the former aggregation can be described by the
two parameters r^ and 1, where r^ is the radius of a sphere equal in
volume to n-spot or a half-side of an equivalent cube, while 1 is the
distance between their centers. With the distribution of n-spots stable
in the probabilistic sense, rp and 1 act as constant means. From the
standpoint of the m-school , tne value of r^ is replaced by the quantity
r = Tf^ + r^, where r^ is the distance from the edge of n-spot to the
point where m-school will reliably detect n-spot (this quantity has a
precise statistical sense.

It can be shown (Fleishman, 1974), that the mean specific ration Rj^
of individuals within m-school is

P y*^"^
R = (l5fil! z)w particles per day (2.35)

m

m

where yn,( meter) is

1, if 1 < r (directed catching)
y^, = min r, 1 = 2.36

■" r, if r < 1 (blind search);

z (in particles/meter) is the energy cost expressed in individuals,
equivalent to the loss of z food particles in one meter of travel path,
w (meter/day) is the mean speed of movement of m-school.

The expression R_ will now be analyzed given the constant value:

N .particles,
^ 'q meters^

Of the mean construction of food and the variable aggregation of food,
defined by the parameter 1 or v = V-/l^.

355

The double representation (2.36) of the value of y^^ results from
the two possible modes of hunting of an active predator seeking passive
prey (we shall not consider the case of a passive filter-feeder, which
simply waits for food to "swim up" to it). We are concerned with the
mode of directed ("visual") search (r > 1), in which n-spots are always
located within the field of detection of m-school, and the school
sequentially consumes the spots, as well as the mode of blind search, in
which m-school finds n-spots by randomly encountering them (1 > r), or
more accurately, by randomly approaching them until the radius of
detection r^ is reached.

The basic formula (2.35) and its various interpretations have been
used for analysis of materials of the 17th cruise of the research vessel
AKADEMIK KURCHATOV. On this cruise, a visual count was made of the
number of flying fish and schools of flying fish (groups of at least ten
fish) in a section along the equator in the eastern Pacific, and the
time intervals between sightings were recorded. Processing of a portion
of these materials (ignoring the individual fish) produced the data of
Fig. 10. These included X(km)--the mean distance between sightings, m--
the mean number of fish in each school, and p(km"^)--the density of the
number of fish. This last quantity is calculated from the first two:

p = m/x2. (2.37)

All means were calculated for a single day. The schools of flying fish
were encountered only west of 120°W, with a clear maximum in their
density at about 135°W. It is probable that this maximum is explained
by an increase in the concentration (mg/meter^) of zooplankton near the
surface, the food of the flying fish. However, data kindly provided to
us by A. G. Timonin clearly show that the biomass of zooplankton in the
upper 100 meter and 10 meter layers is practically constant between 120°
and 155°W ( B = 75 mg/meter^), while the increase in the value of 3 east
of 120°W is located in a zone where the water temperatures are too low
for flying fish (< 21°C). Thus, we must assume that the abundance of
flying fish also depends on the aggregation of zooplankton for a fixed
density P3 = 3/b(meter"-^) , where P3 is the number of zooplankters per
meter^, b is the mean biomass of one zooplankter.

To explain this effect, we applied the theoretical equation (2.35):

2

Rm = (t--2>> (2.38)

Where R^(day"-^) is the mean specific ration of flying fish in a school
of m fish, y = min (1, r), 1 (meter) is the mean distance between
zooplankton spots, r = r^ + r^ (m) , r^ is the mean radius of detection
of a spot by a school, r^ = /P3/P3P 1 is the mean radius of a spot
( P3p > P3 represents increased density of a spot), z(meter"-'-) are the
energy losses of the flying fish in "standard" zooplankters per meter of
travel distance, w(meter/day) is the mean speed of the school.

356

30

!S

L 0

fi

B

0-/0^ /

/.7^

^^^^

__-.^^^

y^^-

50

-

~^----^jr:=^

-^t:;^^^

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n

1

1

,

ISJ-

~c-'

jJO'

//O" w

C y27.i. IS7'/

cloud

Zif././//^

noise

Fig. 10. Experimental data on the distribution of flying fish (A),
zooplankton (B) and phytoplankton ( C) in the region of the equator at
120-150°W. Explanation in text.

357

Since in the case in question all of the values in equation (2.38)
are constant except for y and m, while the value of y is proportional to
1, it leads us to the following theoretical equation:

m = cl'^, (2.39)

Where c is a constant coefficient: for the case in question, c = 7.

Therefore, together with m, according to equations (2.37) and (2.39),

curve p becomes a theoretical function (a quadratic function) of
parameter l--the aggregation of the food.

Experimental comparison of these values was not performed, due to
the difficulty of observing the aggregation of zooplankton. Therefore,
we could judge the spottiness of the plankton only indirectly, on the
basis of the spottiness of the distribution of phy topi ank ton. The
spottiness of phytoplankton in the region of interest to us was measured
by optical methods (based on the absorption of light by chlorophyll) in
two sessions of approximately one hour each (these data were kindly
provided to us by V. N. Pelevin). To estimate the number of spots, a
threshold of 40 units, located in the moddle of the spread of both
curves, was arbitrarily selected. Using this threshold, on the curve
obtained on 26 January 1964, 23 excursions were noted, on the curve
obtained on 27 January--16 excursions. Given the mean speed of the ship
of 30 km/hr, the mean distances between spots of phytoplankton (1) was
defined as 1.3 and 1.9 km, while the mean number of flying fish on these
days (m) was 12 and 23. A numerical count shows good agreement of the
values m and 1 obtained with the theoretical equation (2.39).

The value c = m/1^ ^ 7 was defined for 26 January; for 27 January,
the "theoretical" value of m was 25.3, which differs only slightly from
the observed value (23). Thus, we can present the following theoretical
equation for the density of predators, given constant density p^ = const
of prey, as a function of the aggregation of the prey 1:

P = c(l/X)2

Where c is a constant related p^^, depending on the type of predator and
prey, 1 and X are the mean distances between schools of predators and
spots of prey.

358

PART 2. HUMAN ACTIVITY AND THE BIOLOGY OF THE OCEAN

CHAPTER I. BIOLOGICAL RESOURCES OF THE OCEAN
AND POSSIBILITIES FOR INCREASING THEM

1. Fishery Production of the World Ocean and Its Utilization.
(P. A. Moiseev)

In recent years, many nations of the world have shown increasing
interest in the study and utilization of the biologic resources of the
ocean. This has resulted primarily from an increasing shortage of
animal protein--the most important and irreplaceable component part of
the diet of the rapidly growing population of the world. Even today,
with the population of the planet approaching 4 billion people, more
than one half of the world's people do not receive a sufficient quantity
of animal protein, or even are simply starving. This is particularly
true of the developing nations of Asia, Africa and Latin America (Table
1).

Table 1. Daily consumption of animal protein by the population of the
earth (excluding the Socialist countries), expressed in % of the total
population.

Consumption of Animal Protein

1938

1960

1970

In Weight Units, g
<15
15-30
>30

59.0
18.9
22.1

60.7
19.8
19.5

62.0
20.7
17.3

In Calories

<2200

2200-2700

>2700

38.6
30.8
30.6

59.4
19.0
21.6

63.0
17.0
20.0

Specialists in the area of nutrition believe that the daily
consumption of 30 g of animal protein is sufficient for good nutrition,
while consumption of less than 15 g per day is insufficient and
dangerous for health. Thus, an ever increasing fraction of the world's
population, already more than half, is suffering from chronic
malnutrition.

359

We know that 1 ha of land, given modern methods of cultivation, can
feed 7 people. At present, some 1.4 billion ha of the earth's surface
(approximately lOX of the continental surface) is under cultivation, so
that the fruits of agriculture, given intelligent use and distribution,
could feed 10 billion people. If agriculture were improved and planted
areas expanded, these capabilities could be still further increased.
However, agricultural production, and particularly animal husbandry,
require great efforts and capital investments, which are amortized over
a long period of time. Therefore, the self-renewing biologic resources
of the World Ocean have, in recent decades, become an important source
of nutrition, animal feed, and medical and engineering products.

Year 1800 1850 1900 1960 1970 1975

Population of the

world in millions 800 1000 1550 3000 3635 4000

Catch per person, kg 1.5 2.0 2.6 13.3 19.2 16.9

The volume of the total worldwide catch from the ocean in the early
twentieth century was around 4 million tons, i.e., 2.6 kg per inhabitant
of the earth. The rapid increase in the catch in recent decades has
meant that by 1960, some 40 million tons were taken from the sea (13.3
kg per person), in 1970-1975--65-70 million tons (17-19 kg per
person). At present, products obtained from the seas and oceans account
for 15% of the balance of food proteins, significantly less than the
fraction accounted for by milk and meat. However, a comparison of the
total volume of food obtained by man from the sea and from the land
indicates that the "fields of the sea" provide a more than modest
harvest. About 3% of the surface of the earth-- the area of cultivated
land--provides almost 99% of the food eaten by man, whereas the other
71% of the earth's surface, covered by the seas and oceans, provides man
with slightly over 1% of his food.

According to modern best estimates, each year, some 300-320 million
t of fish and large invertebrates are produced in the ocean, of which
about 90 million t could be caught by man. Thus, there are genuine
possibilities for significantly increasing the catch, but, at the same
time, the demands of mankind are such that by the year 2000 it would be
desirable to obtain as much as 140-150 million t of fish and related
products--that is, twice the present level .

What are the potential capabilities of the World Ocean as a source
of food, to what extent and by what methods can the harvest of the "blue
fields" be increased, and what is the reason for the relatively low
yield of food from the tremendous area of the World Ocean? These
questions must be answered in order to provide an objective evaluation
of the possible volume of commercial production of the ocean.

360

In recent decades, research vessels have made thousands of voyages
to all regions of the World Ocean; hundreds of thousands of fishing
ships are at work each day, catching fish down to depths as great as
2,000 m, at all distances from their bases, using the most modern
equipment available for the detection and catching of commercial
varieties of fish. As a result, an extensive fund of data has been
accumulated concerning the topography of the bottom of the World Ocean,
the oceanographic characteristics of its various regions, and the
regularities of the processes which define the biologic productivity of
the ocean. They allow us to form an approximate idea of the volume of
commercial production formed each day in the World Ocean and the
peculiarities of its distribution and reproduction.

1.1 Productive Regions of the Ocean.

The biologic productivity of the World Ocean and, in the final
analysis, the volume and nature of its commercial production, depend to
a great extent on the relief, hydrological and hydrochemical regimes,
atmospheric processes, balance of nutrients, and on the peculiarities of
the productivity of phytoplankton and zooplankton. We should emphasize
a few facts which are of particular significance for an understanding of
the peculiarities of the production and distribution of the biological
resources of the World Ocean.

Only 7.4% of the area of the ocean is less than 200 m deep, only
11.4% is less than 1,000 m deep. Almost 77% of the area of the ocean is
over 3,000 m deep (Table 2). If we consider that the most extensive
shallow-water areas are located in the Arctic, with a great deal more in
the Antarctic, we find that the total area of regions favorable for
habitation by commercial benthic animals is about 30 million km^--only
8% of the area of the ocean. However, it is the continental shelf and
the waters of the peripheral regions of the ocean which are most
productive and it is this area, 20% of the water area of the ocean,
which acounts for some 90% of the present world catch. This uneven
distribution of the catch is primarily a result of the fact that areas
of high biologic productivity are to be found around the edges of the
oceans.

It has been established in recent years that a significant quantity
of fish, in accumulations dense enough to allow successful commercial
fishing, may be formed in individual areas of the World Ocean far from
the coast, near the slope or over elevated areas of the deep-sea floor
(with depths as great as 2,000 m) . This type of concentration results
from the existence in these regions of an intensive upwelling of deep
water, resulting in the creation of zones of increased biologic
productivity. There is good reason to believe that commercial
concentrations of fish will be found over some of these underwater
elevations, with a total area of about 1.5*10° km^.

The most productive zones, with the daily primary productivity of
about 1.2 g Z/w- and zooplankton biomass of over 100 mg/m-^, cover about
17% of the total area of the ocean. This is approximately the same
level of productivity as that of continental ecosystems--forests and

361

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362

pasture lands. Zones of low productivity, not exceeding the
productivity of deserts, occupies some 63% of the area of the ocean.
The 37% of the ocean occupied by productive regions accounts for over
70% of the primary production. The edible benthos is still more
strongly restricted to the periphery of the ocean, 58% being
concentrated at depths of less than 200 m and 90% at depths of less than
100 m.

According to approximate calculations, the total quantity of
zooplankton accessible to animals of higher trophic levels, principally
fish, is about 6-20 billion tons. The biomass of the benthos is
relatively low, not over 2.5 billion tons within the limits of the
commercial depths (down to 1,000 m) , including about 1 billion tons of
edible benthos.

The results of complex oceanographic and fishing-industry studies
of the World Ocean, undertaken in recent years, have allowed us to
direct the development of Soviet fishing primarily toward the
utilization of the biologic resources of the ocean which, in combination
with the construction of a large, modern fishing fleet, has allowed us
to achieve a rapid increase in the total catch and significant
improvement in the quality of fish products supplied to our
population. At the present time, the sea and ocean fishing industry of
the USSR provides over 90% of the total fish catch eaten in the nation,
and it is assumed that this industry will continue to play a dominant
role in Soviet fishing in the future (Table 3).

Table 3. USSR fish catch (t-lO^).

Catch 1930 1940 1950 1960 1970 1975

Total

1,283

1,509

1,654

3,511

7,775

10,300

In open seas

380

965

945

2,736

6,750

9,168

In internal

waters

903

744

709

775

1,025

1,132

Thousands of Soviet fishing, transportation and processing ships,
utilizing the stock of fish available in the World Ocean, achieved an
increase of the fish catcii of the USSR from 2.7 to 10.3*10° t in 1955-
1975. During these years, some 55 million tons of seafood were
caught. The Soviet catch today represents about 14% of the world's
production of seafood.

The increase in the total catch of sea fish has occurred primarily
on the continental shelf and in the upper portion of the continental
slope, as well as peripheral oceanic regions, especially in the southern
hemisphere, which is less extensively fished. At the same time, there
has been a relative decrease in the significance of traditional species

363

(herring, cod, plaice, sea perch, etc.), a decrease in the significance
of the most important fishing regions of the northern hemisphere, an
increase in the number of species, the reserves of which have been
reduced by overfishing, a decrease in the success of fishing for most
traditional species of fish, and an increase in the importance of fish
with lower or unusual food value (anchovy, pollock, Arctic cod, capelin,
horse mackerel, etc.). The experience of world fishing during recent
decades has confirmed that the intensity of commercial utilization of
many traditional species is near its limit, which, in some cases, has
already caused overfishing, basic disruption of ecosystems and harmful
changes in the genetic structure of populations. The time has come for
commercial use of the biologic resources of the lower trophic levels and
the most rapid possible development of methods for the control of the
biologic processes in the ocean, in order to make the transition from
the current hunting stage of fishing to a controlled fish economy with
stable fish productivity.

The need for man to take an active part in the control of the
biologic production processes, to change their directions and results in
his own interest, is becoming obvious.

1.2 The Level of the Modern Catch.

The mean fish productivity of the World Ocean is relatively low:
in 1967, with a total seafood catch of 60 million tons (including a
correction factor for the catch not accounted for), the productivity, in
terms of the entire surface of the World Ocean, was only 167 kg/km
(Moiseyev, 1969). In 1970-1975, the total catch (including the same
correction factor) approached 70 million tons, averaging 190 kg/km*^. In
the most productive regions, the catch amounts to 0.06-0.07% of primary
production, which is approximately the level achieved in the highly
productive and intensively fished Caspian Sea (0.1%). Special
calculations have allowed us to produce an approximate estimate of the
potential level of fish production of traditional species in the World
Ocean--about 90 million tons (Moiseyev, 1969). Thus, the current catch
of fish and large invertebrates is approaching the limit. The world
catch of fish and other seafood (excluding whales) is presented below
(in millions of tons).

1850

1900

1913

1938

1950

1960

1.5-2.0

4.0

9.5

10.0

21.0

21.1

1965 1970

1971

1972

1973

1974

1975

40.0 71.0

70.9

66.2

66.8

70.5

69.7

364

What is the current level of human utilization of the fish productivity
of the ocean?

Of the total volume of the world catch from the ocean (including
whales), the overwhelming majority--90% in 1974--consists of fish,
followed by invertebrates, then aquatic plants in third place and,
finally, whales in fourth place (Table 4),

Most of these objects (about 90%) are retrieved from the seas and
oceans. Over the postwar period, almost the entire increase in the
world catch had resulted from further utilization of oceanic biologic
resources. Since 1950, when the prewar level of the world fish catch
was reached, through 1970, the catch of sea fish has increased by 35.5
million tons, of fresh-water fish--by only 6.0 million tons. After
1970, the total catch of sea fish significantly decreased (by 5.5
million tons by 1973) as a result of the catastrophic drop in the
population of the peruvian anchovy, while the catch of fresh-water fish
remained almost the same.

At the present time, inhabitants of the pelagic zone dominate
commercial fishing (Table 5).

The catch of pelagic fish during the postwar period has increased
by 27.5 million tons, to a great extent due to the Peruvian anchovy
catch, to the point that it represents 70% of the total catch; the catch
of benthic fish has increased by only 10.5 million tons. Doubtless,
this process is related to some extent to the opening of new regions and
methods to fishing, as a result of extensive research operations, as
well as the improvement of sonar devices for finding schools of fish and
fishing techniques. However, the successful development of pelagic
fishing has resulted primarily from the dominance of the population of
pelagic fish over that of the benthic inhabitants of the sea (Table 6).

Most (75%) of the catch consists of fish which feed on zooplankton
and phytoplankton, 20% consists of predatory fish, predominantly small
predators, while a very small fraction--4%--consists of fish feeding on
the benthos. Planktonophages include the most numerous commercial
fish: herring, anchovies, sauries, Scombridae, Carangidae,
Scorpaenidae, etc. The benthophages include the Pleuronectidae,
Cottidae, etc. The large predators include the sharks, tunas and
swordfish, while smaller predators include the small tunas and many
other fish.

In recent years, commercial fishing of pelagic fish has been
developed primarily with a reduction in the catch of the most valuable
inhabitants of the benthic waters, from the standpoint of food (cod,
plaice, sea perch, etc.) as a result of a reduction in their population
due to intensive fishing. The weight relationship (in %) of the catch
of planktonophagous fish, predators, benthophages and euryphages (based
on data from 1973) is as follows: 75:20:4:1.

Predatory fish feed primarily on planktonophagous pelagic fish,
and, to a much lesser extent, benthophages. If we assume the feeding

365

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366

Table 5. Composition of the world catch of fish by regions (%).

Items

1938

1948

1959

1965

1973

Pelagic Fish
Epi pelagic fish

open ocean
Neritic regions

60.0

5.5
54.5

56.8

4.9
51.9

63.1

10.2
52.9

67.8

6.6
61.2

69.0

5.0
64.0

Benthic Fish
Shelf
Slope

40.0

37.6

2.4

43.2

39.4

3.8

36.9

32.5

4.4

32.2

27.3

4.9

31.0

26.0

5.0

Total

100.0

100.0

100.0

100.0

100.0

Catch, t-103

16,400

15,470

24,880

39.620

46,810

Table 6. Catch of marine fish with various feeding habits.

1940

1950

1960

1973

Fish

t-io6

%

t-io^

%

t-io^

%

t-io^

%

Planktonophages

8.97

59

8.71

57

18.10

62

35.11

75

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0.32

4

0.60

7

6.12

34

8.92

19

Zooplanktonophages

8.65

96

8.11

93

11.98

66

26.19

56

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4.70

31

5.13

34

8.49

29

9.40

20

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1.15

8

1.04

7

2.24

8

1.87

4

Euryphages

0.29

2

0.36

2

0.38

1

0.48

1

Total

15.11

100

15.24

100

29.21

100

46.86

100

367

coefficient to be 7-8, we find that they consume approximately 80 to 90
million tons of planktonophages and about 10 million tons of
benthophages . Thus, the total volume of planktonophagous fish removed
each year by fishing and by the inroads of predators amounts to 120-130
million tons, the total quantity of benthophages lost in these two ways
is about 12 million tons.

The relationship of the production of zooplankton and benthos
available for utilization by fish and other larger animals within the
limits of the peripheral zones of the ocean is about 15:1 (zooplankton
15 billion tons, benthos 1 billion tons). The catch of
zooplanktonophages (including 2 million tons of whales and 1 million
tons of squid) is also at present approximately 15 times greater than
the catch of benthophages. It seems likely that the intensity of
fishing of demersal fish (benthophages) has reached its limit or is
close to it, but there is some possibility for an increase in the catch
of planktonophages, by increasing the catch of the inhabitants of the
pelagic zone of the open ocean, where approximately the same quantity
(15-20 billion tons) of zooplankton is produced as in the peripheral
zones. Analysis of the volume and composition of the world fish catch
confirms this conclusion.

In spite of the great variety of species of fish which are utilized
by the fishing industry, the fate of world fishing is determined by an
extremely limited number of families and species of fish, which have
large populations. Representatives of seven fami 1 ies--the inhabitants
of the continental shelf and the neritic areas of the ocean (the
Engraulidae, Clupeidae, Gadidae, Carangidae, Thunnidae, Pleuronectidae
and Scombridae) provide about 7U% of the world catch of sea fish (Table
7).

The most numerous species, such as the Peruvian anchovy, the
pollock, Atlantic cod an oceanic herring, the Caspian hake, the capelin
and a few species of sardines, yield about 25 million tons in certain
years, which is the majority of the catch of sea fish. The Peruvian
anchovy alone in some years has yielded over 18% of the world catch, and
about 25% of the catch of sea fish.

It is characteristic that in recent years, the catch of many
important commercial fish, in spite of more intensive fishing, has
significantly decreased. Many traditional fishes, which have long been
greatly used as commercial fish, specifically the ocean herring,
Atlantic cod, plaice, and Peruvian anchovy, have shown clear signs of
depression of their reserves, which has directly influenced the volume
of fishing and led to a reduction in the total volume of the world
catch.

Before 1972, the anchovies held first place in the world fish
catch, their 1970 yield reaching 14.6 million t (Table 8). In 1973,
anchovy catch dropped to 4.0 million t.

the

Most of the anchovy catch is represented by the Peruvian anchovy.
In recent years, the catch of cape anchovy and northern Pacific anchovy

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has greatly increased, whereas the catch of North Atlantic, Japanese and
Mexican anchovy has remained at approximately the same level (see Table
8).

Among the Clupeidae, the ocean herring, menhaden, and sardines are
of greatest commercial significance.

The catch of all Clupeidae at the present time consists primarily
of ocean herring (Atlantic and Pacific), with the Atlantic yielding the
greatest number (Table 9). The population of both species fluctuates
widely under the influence of both natural factors and fishing.

In recent years, the reserves of most schools of Atlantic and
Pacific herring have been deeply depressed, their total catch dropping
by 50% between 1966 and 1975, to 2.5'10" t. Such reserves of herring as
the Arctic-Norwegian, Korf-Karaginskiy, Sakhal in-Hakkaido, Gizhiga, etc.
once so numerous have been completely exhausted and no longer support
any significant commercial fishing. There is a real danger that, unless
effective measures are taken in the next few decades, it may prove
impossible to restore many populations of herring, and a further
reduction in their reserves will occur. Some twenty nations are
involved in fishing for Atlantic herring, but the greatest catches
during productive years were those of the USSR (700-780 •10'^ ), Norway
(1.2-10^ t), Iceland (770-10-^ t) and Denmark (280-360-10-^ t). The
Pacific herring is caught primarily by the USSR (320-460 -lO^ t), Japan
(about lOO'lO-^ t) and Canada. The 1 ittoral-estuarine menhaden is found
along the Atlantic coast of the USA and in the Gulf of Mexico, is fished
exclusively by American fishermen and is used for the preparation of
nutrient flour.

Sardines are traditionally fished by Portugal, Spain, Morocco,
France, Italy and other countries; the size of the sardine catch has not
significantly changed in recent years (Table 10).

Furthermore, beginning in 1971, an increase has occurred in the
population of the Japanese sardine or ivasa, which, during the prewar
years (1939-1940) supported an annual catch of about 2 million tons. In
1976, its catch reached 0.8 'lO" t, and there is every reason to believe
that it will continue to increase in the future. However, in the next
few years, as a result of further reduction in the catch of sardines and
sardinella off the coast of Africa, the decrease in the population of
Atlantic and Pacific herring, the decrease in the total world catch of
Clupeidae will continue. Only the organization of fishing for Clupeidae
off the coast of South America and Australia, plus an increase in the
catch of the Japanese sardine, can stop this process. Since 1972, the
Gadidae have occupied first place in world fishing, primarily due to the
increase in the catch of pollock, tresochka esmarka, saithe and several
species of hake (Table 11).

The catches of Atlantic and Pacific cod, composing one-third of the
total catch of Gadidae, have been greatly reduced as a result of the
depression in the stock of fish in the Atlantic. The catches of far
eastern cod have increased somewhat, but are far from the potential

370

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372

possible reserve.

The catch of hake almost doubled in 1965-1973. However, in spite
of the great intensity of fishing, the catch of most species of hake
(silver hake, patagonian hake and European hake) has decreased or held
steady. The supply of hake along the Pacific coast of North and South
America is still in good condition, as is the reserve off the coasts of
South Africa.

The catch of Pacific pollock, now widely used for the preparation
of nutrient flour and stuffing, is rapidly increasing; the catch of this
fish is now approaching 5 million t, 80% being accounted for by Japan.
In recent years, the stock of pollock in Korea Bay and Petr Velikiy Bay,
off the coast of Hokkaido, Sakhalin, Kamchatka and in the eastern
portion of the Bering Sea, has been intensively used. We must assume
that no less than 10 million tons of pollock are consumed by the Pacific
Ocean seals each year. Reports are already being heard of significant
decreases in the average age of many populations of pollock; therefore,
a further increase in catch can occur only if the populations of the
northwestern portion of the Bering Sea and the Gulf of Alaska, still
incompletely utilized, can be brought into play.

The catch of other Gadidae can be significantly increased by
development of fishing for hake within the regions mentioned above, as
well as the eastern Pacific, off South Africa and the Patagonian Shelf,
by fishing for poutassou in the North and South Atlantic, and Arctic cod
in the Barents Sea. At the same time, the catch of cod, haddock, silver
and red hake in the traditional fishing regions of the North Atlantic
will decrease, while the total catch of pollock and hake in the Pacific
Ocean will remain at approximately its present level. The number of
commercial species of Gadidae as yet plays a secondary role in
commercial fishing: whiting--catch up to 270 -lO^ t, tresochka esmarka--
up to 900 -lO^ t, tusk--30-50«103 t, poutassou--40-80«lo3 t, etc.,
although in most cases the size of the catch does not correspond to the
population of these fish at all. This is a result of the low economic
effectiveness of fishing for these species, due to the relatively low
quality of their meat.

The development of sea fishing with the extensive use of trawls at
different depths, purse seines, longlines and other hook equipment has
led to a rapid increase in the catch of a number of pelagic fish,
including many species of the Carangidae and Scombri dae. At the present
time, both of these groups support a total catch of about 5 million
tons, significantly greater than the catch of Thunnidae, Salamonidae,
Pleuronectidae, etc. The catch of Scombri dae has increased from 1.3' 10°
t in 1965 to 3.2 '10° t in 1975. Representatives of this group inhabit
primarily the neritic zones. Of the world catch of Scombridae, 56%
consists of the Japanese mackerel, 34% of the common mackerel and 10% of
the Indian mackerel (data for 1973). A significant fraction of the
catch of mackerel is taken by Japan--up to 1.4»10° t, while a large
quantity, as much as 480 'lO-^ t is caught by Norway, significantly less
by the USSR, France and South Africa. The extremely rapid growth of the
Norwegian catch of mackerel (from 23,000 t in 1963 to 480,000 t in 1966)

373

is explained by the high population of this fish off the coast of Norway
and the use of purse seines, which accounted for 455,000 t. The Soviet
Union has greatly intensified its fishing for mackerel in recent years,
in the northwestern Pacific (to 80,000 t) and off West Africa (to
150,000 t) . Doubtless, mackerel fishing is quite promising.

The catch of Carangidae had increased by a factor of 16 by 1970 in
comparison to the prewar level (1938), and there is every reason to
assume the possibility of further increases. Thus, off the coast of
Japan in some years the catch of this fish has even been artificially
held down. Large accumulations of mackerel have recently been found off
the Tasmanian coast. In the opinion of many scientists, it will be
possible to catch as many as 1 million tons of pelagic fish per year
near New Zealand, including many Carangidae. The greatest quantity of
Japanese mackerel are caught in the East China Sea and off the coast of
Japan (510-560«10-^ t), as well as in the Philippines (lOO'lO^ t) . Other
species of Carangidae are caught off the west coast of Africa, where
fishing is conducted primarily by ships of the USSR (ISO'lO-^ t) , Angola
(170 .10^ t) and Spain (70 -lO-^ t).

A lesser role in the sea fish catch (up to 1.7'10" t) is played by
the tuna, although due to the high value of the meat of this fish, tuna
fishing is significantly more successful economically than fishing for
most other types of fish. Therefore, the tuna catch develops from year
to year, and at the present time is conducted in the open Pacific,
Atlantic and Indian Oceans. Tuna inhabit the great water areas of the
ocean, forming no dense accumulations, making it more difficult to catch
them. However, information on the results of tuna fishing indicates
that the trend is doubtless toward decreasing effectiveness (Table
12). For example, the catch of yellowfin and blue-finned tuna decreased
from 8 fish per 100 hooks on a longline in 1950 to 2 in 1965. The
reserves of large tuna are being caught with great intensity in almost
all regions of the ocean, and the only hope for any significant
development of tuna fishing lies in more intensive fishing of the
smaller and stripe-bellied tuna.

The overwhelming majority of tuna (50-60%) is caught by Japan.
Significantly smaller quantities are caught by the fisherman of the USA,
France, Spain and Peru. The Soviet Union catches but a few thousands of
tons of the valuable fish.

When tuna is fished using longlines, swordfish and sharks are
caught in large quantities. Sharks, rays and chimaera are also the
objects of a specialized fishing industry. The annual catch of sharks-
in recent years (1968-1975) has held steady at a level of about 400' 10"^
t, of rays at 90-140 -lO-^ t. This is much less than their actual
reserves. The shark catch in the World Ocean could be at least doubled.

In addition to the commercial fish mentioned above, the world catch
includes many representatives of various families of demersal fish,
caught during trawling and other types of bottom fishing:
Pleuronectidae (see Table 8), sea perch, Ammodytes, etc. (Table 13).

374

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The overwhelming majority of these fish, inhabiting the shelf or
the upper portion of the slope, have long life cycles and relatively low
reproductive capacity which, in combination with intensive fishing, has
led to a decrease in the population of many species of fish,
particularly the plaice and sea perch. Doubtless, a significant
increase in the catch of certain benthic fish, such as sand eels, is
possible. However, the fact that the overwhelming majority of these
species are littoral, shallow-water fish which fomi significant numbers
of small, local populations, makes this group of fish suitable primarily
for coastal fishing.

There are other fish which are promising for the development of
fishing. They include primarily representatives of the Sauridae--the
sauries, widespread in the North and South Atlantic and in the Pacific
(saury fishing is being successfully conducted by Japan and the USSR,
bringing in as much as 300-500"10^ t in some years). No less promising
is fishing for capelin, the catch of which in the Sea of Norway and the
Barents Sea and in the region of Newfoundland has exceeded 200 million
tons in recent years. Representatives of the family Myctophidae are
also quite numerous, with large accumulations of these fish found by the
bottom and depths of 500-900 m in various regions of the ocean,
particularly off the Pacific coast of Japan.

The invertebrates are of much less significance in the world
seafood picture, representing about 8X (5.8 -lO^ t) of the total world
seafood catch. Of this quantity, 65-70X consists of mollusks, about 30%
(1.9*10" t) crustaceans, and about 70*10^ t of Echinodermata and
others. The world catch of invertebrates is growing slowly (Table 14).

Mollusks are caught in the largest quantity off the coast of
Japan--up to 1.4-1.6'10° t, primarily squid and bivalves. A large
quantity (0.6-0.7'lp° t) of mollusks is caught in the USA, mostly
oysters (0.3-0.4-10° t) , abalone (0.2-10° t) and scallops (0.1-10° t).
The USA takes approximately half of the entire world catch of oysters,
Japan and France representing a large fraction of the remaining catch.
Mussels are caught primarily by European fishermen (about 85% of the
total catch) predominantly from the Netherlands (up to 120-10^ t) ,
Spain (70 -lO^ t) and France (30-40-10-^ t). One of the most valuable
mollusks is the scallop, which is primarily caught in the northwestern
Atlantic off the coast of the USA by fishermen from Canada (60-70-10^ t)
and the USA (70-80-10^ t). A significantly smaller quantity of scallops
(about 7,000 t) is caught by Japan and by Australia. The prospects are
obviously favorable for the development of the mollusk fishing industry,
particularly squid, as well as small bivalve mollusks (used as feed in
animal husbandry) in many regions of the ocean.

Among the crustaceans, first place is occupied by shrimp. The
largest catches are brought in from the Gulf of Mexico, the Caribbean,
the coasts of Japan and India, and the Bering Sea. Following shrimp, in
terms of catch, are the crabs (primarily the Kamchatka crab), then the
lobsters. The intensity of fishing for the Kamchatka crab and the
lobster threatens depletion of the reserves and requires that additional
measures be taken to regulate fishing. The resources of shrimp and

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377

Atlantic lobsters will allow the catch to be increased in a number of
regions.

The annual catch of Echinodermata is about 70,000 t, of which some
60% consists of sea urchins.

Marine vegetation--algae and marine grasses--are taken in large
volumes from the shallow waters of the World Ocean (about 1.2«10" t) ,
about 70% being grown and taken in Japan.

As concerns the whales, due to the great decrease in the population
of the largest toothed whales--the blue whale, fin whale and humpback
whale--in recent years fishing for smaller whales has been developed,
primarily the sei whale and minke. The total weight of whales caught
decreases from year to year.

This, in general terms, is the current volume and composition of
the catch of seafood in the World Ocean.

The current level of intensity of utilization of the reserves of
most traditional hunted objects in the World Ocean, in many cases, is
quite high, but in many regions it can be significantly increased.

Analysis of the information we have presented shows that the
intensity of commercial utilization of most of the main commercial
species of fish, particularly the cod, sea perch, plaice and herring,
which are the most sought-after fish in the northern hemisphere, has in
most regions reached or almost reached its limit, and any increase in
the catch will occur only as a result of an increase caused by such
natural factors as may increase the population of individual generations
making up the total world population. This is particularly true of the
northwestern and northeastern sections of the Atlantic, and the northern
and north-central sections of the Pacific. Naturally, the catch of such
demersal fish as the macrourus pollock, Arctic cod. Pacific cod and
certain other benthic fish may be increased even here. However, this
increase will be relatively slight and can only compensate for the
decrease in results of fishing in the most important regions to a small
extent.

The greatest increase in the catch of benthic fish can be expected
primarily within the tremendous area of the Falkland-Patagonian
shallows, where the catch of hake, poutassou, macrourus and certain
others may become as great as 3 million tons. The New Zealand plateau,
the eastern and southern coasts of Australia and the Pacific coast of
South America represent smaller, though still significant possibilities
for increasing the catch of benthic fish. All remaining regions in the
World Ocean can provide only a slight increase in the catch of benthic
and deep-water fish in comparison to the levels already achieved. The
total possible increase in the catch of benthic and deep-water
inhabitants within the relatively shallow areas of the World Ocean may
be about 4-5 "lO" t, of which most will come from the regions which we
have already mentioned. A significantly greater increase in the catch--
up to 17-20 'lO" t--can be expected from the catching of fish and other

378

animals which lead a pelagic mode of life and primarily inhabit the
highly productive neritic areas and the adjacent portions of the oceanic
zone. These are primarily sardines and other similar species,
anchovies, Carangidae, Sauridae, small tunas, Myctophidae, squids and
certain others. Judging from the level of use of these animals achieved
to date in some of the neritic regions of the ocean and data on their
distribution and population in other regions, we can assume the
possibility of a significant increase in their catch in all oceans,
particularly off the coast of Australia, in the northern, west-central
and east-central parts of the Pacific and southwest Atlantic oceans.
The prospects for the central oceanic regions are more limited.

Judging from the status of the biologic resources of the World
Ocean, we can present the following, quite approximate figures for the
probable increase in the world catch of the most important groups of
ocean fish (Table 15) .

Table 15. Probable increase in world seafood catch (t'10°).

Group

Pelagic species

Engraul idae

Clupeidae

Carangidae

Scombri dae

Sauridae

Thunnidae

Euselachiae

Teuthoidea

Other
Benthic objects

Gadidae

Pleuronectidae

Macruridea

Other (including
invertebrates)
Total

In most regions, the probable increase in catch will occur
primarily due to an increase in the catch of inhabitants of the upper
portion. of the slope and elevations of the ocean floor--macruri ,
macruroni, hake, lemonema, etc., in warm-water regions of the shelf--due
to an increase in the catch of the numerous species of Carangidae,
Sciaenidae, etc. To a significantly lesser extent, we can expect an
increase in the catch of poutassou, saithe, haddock, pollock, cod and
hake. A significant increase in the total volume of the catch may be
accounted for by inhabitants of the waters of Australia and New

379

1974

Probable Increase

Probable

Catch

in Catch

Catch

38.3

21.0

59.3

6.0

7.0

13.0

7.7

1.7

3.0

2.5

2.1

4.6

3.2

0.3

3.5

0.5

2.0

2.5

1.7

1.1

2.8

0.6

0.4

1.0

1.1

2.9

4.0

15.0

1.5

18.9

21.7

5.7

27.4

12.7

2.3

15.0

1.2

0.0

1.2

0.6

0.9

1.5

7.2

2.5

9.7

60.0

26.7

86.7

Zeal ancl--Beryci formes, etc. In the neritic zone, most promising for the
development of fishing are the Engraulidae, Carangidae, Scombri dae,
sardines, and, in adjacent regions of the oceanic zone--sman tuna,
sauries, Myctophidae, Teuthidea and certain other species. Finally, in
the oceanic zone itself (in the epipelagic zone), the most important
objects for a developing fishery may be the large and small tuna,
marlins, swordfish, dorados, sauries, sharks, flying fish and squids.
Thus, the prospects for the development of world fishing can be rather
clearly seen--primarily due to an increase in the catch of pelagic
seafood.

In spite of the exceptionally great quantity of certain species of
anchovy currently taken from the ocean, we can expect an intensification
of anchovy fishing off the coasts of Argentina and Mexico, which may
yield approximately 3 million tons. We should keep in mind that the
population of anchovies and sardines is subject to great fluctuations
and, therefore, the possibility must be considered of great, at times
catastrophic, decreases in the catch, as has occurred with the Peruvian
anchovy, Japanese and California sardines. There are doubtless
possibilities for increasing the sardine catch and the catch of similar
forms near the coast of Africa and Australia, and also of certain
species of Carangidae and Scombridae in various regions of the ocean.
There is every reason to believe that in the epipelagic zone of the
northern and southern areas of the Pacific and Atlantic Oceans, there
are large numbers of Sauridae, of which the northern Pacific saury,
perhaps, is the most numerous. If we can find effective methods for
creating artificial concentrations of this fish in open regions of the
ocean, where it is quite scarce, the saury catch may be significantly
increased.

A significant increase in the catch may also occur by the
development of the catch of small tuna, the reserve of which is as yet
underutilized in many regions of the ocean. There is no reason to
expect a great increase in the catch of large types of tuna. The shark
catch can be doubled, but the total volume of this catch will not be
high in the near future.

Among the pelagic fish promising for fishing purposes we must
include the capelin, flying fish, Australian salmon, dorados,
Myctophidae, etc. Fishing for squid seems quite promising, since the
reserves of this animal would allow its total catch to be increased by
many times.

More intensive fishing for pelagic animals would allow an increase
in the catch by 20-25 million tons.

1 . 3 Regional Placement of Marine Fish

The geography of the world fishing industry, i.e., the use of the
raw materials base in various regions, like the fluctuations of the
numbers of commercially fished objects and the status of their reserves,
can influence the composition of the catch and the results of fishing.
Contemporary fishing-economy statistics are based on the division of the
World Ocean into statistical regions by the FAO.

380

As we present the fishing-economy characteristics of the most
significant regions of the World Ocean, we shall use these generally
accepted divisions (Table 16).

Fishing is conducted with the highest yields in 4 regions of the
World Ocean: the North Atlantic, North, West-central and Southeastern
Pacific, the total area of which represents some 26% of the total water
area of the oceans, but yields some 80% of the total world catch.

The Atlantic Ocean is the most productive of the 3 oceans. In
1970, the catch taken from the Atlantic Ocean totalled 26 million tons,
for a fish productivity of 260 kg/km^, significantly higher than the
productivity of the Pacific Ocean (170 kg/km^) or Indian Ocean (40
kg/km^).

The Northeastern Atlantic, including the North Sea, Baltic Sea, Sea
of Norway, Barents Sea and White Sea is a traditional, exceptionally
productive fishing region in the World Ocean. About 60% of the water
area here covers depths of less than 1,000 m. The total catch here
exceeded 11 million tons, doubling since the war, and now represents 20%
of the world catch. This region is particularly important for the
fishing industry of the USSR (Table 17).

The catch in this region increased until 1966. In subsequent
years, as a result of the great decrease in the reserves of herring and
cod, the total catch of all countries has stabilized. The intensity of
fishing for most species has reached the saturation point and only the
poutassou, Scombridae, Arctic cod, capelin and certain other fish can
increase. The total catch of the Soviet fishing industry in this region
in 1974 reached 2 million tons.

North Sea--one of the most productive regions of the World Ocean.
The high biomass of the benthos and zooplankton, consisting primarily of
edible species, and the predominance in the composition of the
ichthyofauna of rapidly growing planktonophages and benthophages, with
the limited population of predators, assure high fish productivity
which, in combination with other favorable conditions, allows the
fishermen of many countries to achieve high and comparatively stable
catches and to increase the yield of fish products per unit area to a
very high level (5.5 t/km^), approaching the first productivity of the
Azov Sea prior to the regulation of the runoff of the Don and Kuban'
Rivers (8.2 t/km^). Of all commercially fished seafood, the pelagic
planktonophagous fish, primarily herring, sprat, and mackerel, occupy
the leading position. Among the benthic, primarily benthophagous fish,
the plaice and Gadidae (cod, haddock, whiting, saithe, tresochka
esmarka) and others are most numerous. Most fish caught in the North
Sea are permanent inhabitants of the Sea, but a certain small quantity
enters the Sea through La Manche (mackerel ) and from the Sea of Norway
(herring of the Norway stock).

Fishermen of many nations fish the North Sea, including those of
the USSR. The Soviet catch in some years approaches 500,000 t (1973--
230,000 t). It consists primarily of herring, sprat and haddock. The

381

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383

degree of commercial utilization of the fishing resources of the North
Sea, particularly herring, is approaching the ultimate limit.

Baltic Sea. The fisb productivity of the Baltic Sea is relatively
low, slightly over 1 t/km^. Some 0.7 -lO" t of fish are removed from the
sea each year, including 0.3 '10° t by the USSR. The commercial
ichthyofauna of the Baltic Sea consists primarily of massive
planktonophages--the Baltic herring and sprat, Baltic cod, feeding on
macroplankton and benthos, plus typical benthophages--the plaice.
Furthermore, we also find salmon, whitefish, vimba, eel, etc. The fish
resources of this sea are rather intensively utilized. The fish
productivity of its individual regions differs greatly: in Botnicheskiy
Bay, it is 0.5-0.6 t/km^, in Kurshskiy Bay, about 9 t/km^. In 1973, the
countries surrounding the Baltic Sea signed a convention calling for
joint development and application of measures for the regulation of
fishing in order to assure efficient utilization of the biologic
resources of the sea.

Barents Sea. The abundance of food in the form of benthos and
plankton, in combination with the favorable oceanographic
characteristics, makes the Barents Sea a region of permanent residence
or seasonal feeding of Arctic fauna (Arctic cod, saffron, cod, polar
plaice), Subarctic fauna (capelin) and Boreal fauna (cod, haddock,
saithe, herring, sea perch, common plaice, etc.). More warm-water fish
also find their way here: mackerel, whiting, etc. Representatives of
the Arctic fauna inhabit primarily the cold-water eastern regions of the
sea, while the Boreal species remain in the more warm-water western
sections.

The cod, haddock, Arctic cod, sea perch, herring and capelin are of
predominant significance for fishing, making up as much as 95% of the
total catch. The catch of the USSR in 1968-1969 reached 0.6-10^ t, then
greatly decreased in subsequent years as a result of a significant
decrease in the population of herring from the Arctic and Sea of Norway,
cod, haddock and sea perch. At the same time a significant increase has
been observed in the population of Arctic cod and capelin, the total
catch of which by fishermen of all nations reached 2 million tons in
1970-1975.

The northeast portion of the Atlantic Ocean also includes the Sea
of Norway and the Greenland Sea, the waters of Iceland, Ireland and the
Bay of Biscay, that portion of the Atlantic adjacent to the Iberian
Peninsula, as well as the open regions of the ocean. Here we find
herring, cod, haddock, sea perch, mackerel, poutassou, sardines, squids,
etc. Very intensive fishing of herring from the Arctic and Sea of
Norway, particularly the huge catch of small, immature fish by Norwegian
fishermen, the so called "fat" herring, has led to exhaustion of the
reserve of this once most numerous stock of ocean herring and
practically complete cessation of fishing within the limits of the Sea
of Norway. Only in recent years has some increase in the population of
herring in these waters been observed.

384

The level of utilization of the raw materials available to the
fishing industry in this region is rather high, and, for many species
(herring, cod, sea perch, plaice, etc.), the maximum possible level has
already been reached, or perhaps even exceeded. Steps are being taken
to regulate fishing through various international conventions and
agreements on fishing. However, this highly productive region of the
World Ocean may slightly increase the volume of its production by the
development of fishing of certain underutilized species: poutassou,
capelin, saithe, mackerel, squids, etc.).

Northwest Atlantic. An exceptionally important fishing region with
a total area of 4 million km'^, of which 27% is made up of water less
than 1,000 m in depth.

For many centuries, accumulations of cod have been fished off the
banks of Newfoundland, and beginning in the mid 1950' s, very intensive
fishing off Georges Bank was begun, taking herring, sea perch, haddock,
silver and red hake, plaice, halibut, macruri, capelin, squids, etc.
(Table 18).

In recent years, the results of fishing here, in spite of a
significant increase in fishing efforts, have not only not increased,
but, in terms of certain species (sea perch, silver hake, etc.) have
even decreased. The current catch (4.0-4.7 -lO" t) has almost reached
the maximum possible level.

Soviet fishing occupies a significant place in the total catch,
utilizing primarily the resources of cod, silver hake, sea perch,
herring, macruri, capelin, etc. By 1974, the Soviet catch reached
1.16 '10° t (over 30% of the total catch). Soviet fishing studies have
revealed accumulations of sauries in the southern portion of this
tremendous region, the population of which is high, and fishing for
which seems quite promising.

Also promising is fishing for squid, which form great
concentrations along the shores of Newfoundland, on the shelf off Nova
Scotia, Georges Bank and in the region of New York.

Intensification of the catch of sauries, capelin, squid and other
little-used fish and invetebrates will allow some increase in the total
volume of the catch. The development of recommendations for efficient
and effective utilization of the fishing resources is the job of the
International Commission on Fishing in the Northwest Atlantic.

The Central Atlantic. Among the commercial seafood in this area,
the inhabitants of the pelagic zone predominate--sardines, horse
mackerel, mackerel, tuna, etc. Among the fish leading a benthic mode of
life, the Cyprinidae (carp) and Sciaenidae predominate. About 5 million
tons of seafood is caught in this area, primarily sardines, mackerel and
sea carp.

In 1974, the Soviet catch was 1.17-10^ t, about 12% of the total
catch of the USSR and 15% of the total catch of all countries in this

385

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region. The low level of fish productivity of this tremendous ocean
region means that the take of fish products at the present time averages
about 180 kg/km^, an order of magnitude less than in the northeast
portion of the ocean. In the most productive areas--the Caribbean, Gulf
of Mexico, near the Antilles, off the northwest coast of Africa and in
the Gulf of Guinea--the catch rises to 400-500 kg/km^. Studies have
shown that the current catch in the tropical zone of the Atlantic Ocean
could be almost doubled.

The South Atlantic has an area of 47 million km^, of which 10.2% is
represented by depths of less than 1,000 m. The shallowest plateau
(about 1.4'10^ km^) is the Patagonian-Falkland shelf, adjacent to the
Atlantic coast of Uruguay and Argentina. The great extent of this
region in latitude allows both warm-water (tuna, marl in, swordfish,
sardines, etc.) and cold-water (poutassou, hake, nototheniids) fish to
live here. The intensity of fishing is high only along the southwest
and south coasts of Africa, where sardines are caught in large
quantities (0.7 -lO^ t), as well as anchovies (0.4 •10° t) and hake
(0.8 'lO" t), whereas on the Patagonian shelf, the fish resources of
which would allow up to 5-6 million tons of fish to be taken each year,
fishing is little developed (only about 0.6* 10" t are removed each
year). The total catch of the South Atlantic is about 4 million tons,
the total possible catch--over 9 million tons. In recent years, the
Soviet trawler fleet off the southwest coast of Africa has caught 400-
720«10'^ t of fish, primarily hake and horse mackerel.

The regions near the Antarctic, inhabited by commercial quantities
of whales, seals, certain fish and particularly small planktonic
crustaceans--krill--are of great significance for fishing. Of the fish
which have or could have commercial significance in the Antarctic
waters, we need note only the species of the nototheniids, and white-
blooded fish. Furthermore, during the warm season, poutassou reaches
this area from the southern portion of the Patagonian shelf, attracted
by the large concentrations of krill, used as food by almost all the
inhabitants of the Antarctic, particularly the whales. The reserves of
krill here are tremendous, amounting to many hundreds of millions of
tons. Whales alone, during the period of their high population,
consumed over 100 million tons of krill each year.

Summarizing the estimate of the raw-material basis for the fishing
industry in the Atlantic Ocean, we should note that the catch of all
countries in this basin can be increased to 36-37 million tons, 10
million tons greater than the current level (as of 1973). The Soviet
Union catches about 5 million tons in the Atlantic, i.e., 63% of the
total catch of ocean fish.

The Pacific Ocean provides up to one half of the world catch of
seafood (27-35 million tons. Table 19). The catch here is dominated by
pelagic objects (89%, as opposed to 55% in the Atlantic Ocean). The
current level of fishing productivity of the Pacific Ocean (170 kg/km^)
is lower than that of the Atlantic Ocean (260 kq/knr) and the
possibilities for further increasing the catch are considerable.

387

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388

In the northern portion of the ocean, to the north of 40°N and in
the adjacent seas, 19.2 '10" t of seafood is caught (1975 figures) i.e.,
two thirds of all the catch of the Pacific Ocean. Soviet fishermen
catch the predominant portion of their total Pacific Ocean basin catch
here (98% in 1974), their catch representing about 3 million tons, or
15% of the total catch in the region. This catch is represented
primarily by Pacific herring, sardines, anchovies, sea perch, cod,
saffron cod, pollock, saury, Pacific salmon, many species of plaice and
halibut, mackerel, horse mackerel, macruri, etc.

Research and prospecting work has allowed commercial exploitation
of previously untouched resources in the Sea of Japan, the Sea of
Okhotsk and the eastern portion of the Bering Sea, near the Aleutian
Islands, in the Gulf of Alaska, along the Pacific coast of Canada and
the USA, in the region of the northwest ridge, along the coast of Japan
and in the open regions of the ocean. This has allowed a significant
lengthening of the list of commercial fish, which now includes many
dozens of species.

The Sea of Japan. The commercial ichthyofauna of the northwest
portion of this sea consists of cold-water forms: saffron cod, pollock,
cod, herring, plaice, mackerel, etc. Warm-water species predominate in
the south: mackerel, saury, anchovies, etc. Up to 1940-1941, Pacific
sardines entered the Sea of Japan in large numbers and their catch by
Soviet, Korean and Japanese fishermen reached 2 million tons. In recent
years, as a result of a change in oceanographic conditions in southern
Japan, where the fish spawn, the number of Pacific sardines has greatly
decreased. In the past few years, an increase has been observed once
again in the stock of Pacific sardines, and in 1975 its catch off the
coast of Japan reached 800,000 tons. Before 1943, the catch of another
massive fish in the Sea of Japan— the herring of the Sakhalin-Hokkaido
stock--was as great at 500,000 tons; now it has decreased to a few tens
of thousands of tons, which has, to some extent, been the result of
natural factors, but to a considerably greater extent, a result of the
excessive overfishing of the spawning herring.

The total catch of all seafood in the Sea of Japan exceeds 1
million tons, mostly pelagic species such as mackerel, horse mackerel,
anchovy, etc. (over 0.6*10^ t) , to a significantly lesser extent (about
0.4'10^ t)--benthic species. The fish productivity of the sea is rather
high: 830 kg/km^ of benthic fish and about 70 kg/km^ of pelagic fish.
Further intensification of fishing can be achieved by some increase in
the volume of the catch of Pacific sardines, horse mackerel, sauries and
other fish in the southeastern portion of the sea.

Considering the warmth of the sea, there are great possibilities
for the development of commercial growth of aquatic plants (sea cabbage,
red laver, etc.), as well as the breeding and raising of invertebrates
(scallops, mussels, oysters, trepangs) and fish.

The Sea of Okhotsk, with the exception of the most southern
portion, is a cold-water sea, its ichthyofauna consisting of forms which
live at relatively low temperatures. The most plentiful commercial

389

objects are pollock, herring, cod, saffron cod, plaice, the Ammodytes,
sea perch, Pacific salmon (chum salmon, humpback salmon, blue-back
salmon, silver salmon, king salmon), Kamchatka crabs, beetle crabs,
etc. Herring and pollock are particularly numerous here. The total
catch reaches 1.6-1.8«10° t. Soviet fishermen, in recent years, have
achieved catches in the Sea of Okhotsk up to 1 million t, primarily of
pollock (450,000 t), herring (300,000 t), salmon (50,000 t), plaice and
crabs. Seals which cluster along the southeast coast of Sakhalin and
Tyuleniy Islands are hunted. In recent years, there has been a
significant decrease in the population of Okhotsk Sea herring (Okhotsk-
Ayansk, Gizhiginsk, Eastern Sakhalin), due to natural factors, greatly
intensified by the effects of heavy fishing. Since the 1960's, a
significant reduction in the reserve of Pacific salmon has occurred,
primarily due to large-scale fishing by Japan.

The current fish productivity of the Sea of Okhotsk is as great as
1,300-1,400 kg/km^. Further significant intensification of fishing is
impossible, and the results of fishing can be high only in years when
the population of herring, pollock and salmon is large, and also as a
result of more complete utilization of the raw-material resources of
cod, Ammodytes, saffron cod, cape! in, mackerel, etc.

The Bering Sea. The commercial ichthyofauna consists of cod,
pollock, Arctic cod, herring (Korf-Karaginskiy and Eastern Bering Sea
stocks), plaice, halibut, sea perch, mackerel. Pacific salmon, capelin,
macruri, and coalfish. Kamchatka crabs are found in large numbers, as
well as beetle crabs (particularly in the eastern portion of the sea and
in Olyutorskiy Bay) and shrimp. Seals nest along the Pribyl and
Komandorskiy Islands, as well as on ice floes. Within the Bering Sea,
fishing is conducted by the USSR, Japan, and the USA each year taking
over 3 million tons, primarily of pollock (2.2'10° t), salmon (50«10'^
t), herring (130-lo3 t), plaice (120 -lO^ t), sea perch (lOO-lO^ t) ,
crabs and shrimp. The Soviet Union accounts for 500-700*10^ t.

The biological resources of the Bering Sea are quite intensively
utilized by fishermen, and most species (plaice, sea perch, salmon,
Kamchatka crabs) are under stress. The volume of fish production on the
shelf is over 1,500 kg/km^, in the pelagic zone--500 kg/km^, i.e., it
reaches the levels found in the most productive regions of the World
Ocean. A further slight increase in the catch is possible by
utilization of the resources of Arctic cod, capelin, mackerel, cod and
pollock.

In the relatively warm-water regions of the Northeast Pacific
Ocean, from the Gulf of Alaska to California, we find sea perch,
pollock, cod, herring, sauries, plaice, halibut. Pacific hake and
salmon. Fishing here is primarily concerned with salmon, herring, sea
perch, plaice, halibut, hake, crabs and shrimp. The total catch reaches
600-700 'lO-^ t, Soviet fishermen, primarily fishing for hake, sea perch,
coalfish, plaice, etc., bringing in about 250«102 t. Further
development of fishing must be achieved here by intensification of
fishing for hake and squid, organization of fishing for sauries, etc.,
with simultaneous limitations of the scale of fishing for sea perch,

390

herring, plaice and halibut, the resources of which are already being
quite intensively exploited. The significant possibility for
development of saury fishing in the open regions of the ocean from the
north coast of Japan to the Pacific coast of the USA is indicated by the
information from fishing research studies and prospecting work
undertaken in recent years.

The total volume of the catch in the North Pacific Ocean can be
significantly increased by fishing for pelagic species (saury, capelin,
sand eels, squids, etc.), the reserves of which are still underutilized.

The central portion of the Pacific, from 40°N1 to 10°S, includes
water from Japan and New Guinea to California and Central America. In
the western part of this region, primarily in the littoral zone, 5
million tons of fish, invertebrates and algae are taken, over 8% of the
total world production. A tremendous assortment of animals and plants
is taken here, including Sciaenidae (large and small yellow perch),
anchovies, Scombridae, Carangidae, Thunnidae, Clupeidae, Euselachiae,
rays and other fish, as well as squid, octopuses, cuttlefish, bivalves
and Gastropod mollusks, shrimp, lobsters, crabs, sea urchins,
Holothurioidae and other invertebrates, the share of which, for example
in the Japanese catch, is as high as 30%. Furthermore, large quantities
of bivalve mollusks are raised off the coast of Japan, then used as food
and for the production of pearls, and as much as 500,000 tons of seaweed
is raised as food.

The high biologic productivity and utilization of the most varied
representatives of marine fauna and flora have led to the fact that the
total fish production on the shelf along the east coast of Japan is as
high as 1,300-1,500 kg/km^, in the pelagic zone--l, 200-1, 300 kg/km-^,
i.e., significantly greater than the equivalent figures for most other
regions of the World Ocean. Some increase in the volume of the catch
here is possible, by intensification of the fishing of saury, horse
mackerel, anchovies, small tuna and squid, and also by organization of
catching of myctophids.

In the east central Pacific, near California, Mexico and Central
America, fishing is relatively little developed, not nearly
corresponding to the resources of this region. Only about 1 million
tons is taken from this region, primarily tuna, marl in, mackerel and
some benthic species of fish, the production per unit area being only
about 20 kg/km^. However, tremendous accumulations of anchovies have
been found here, allowing a catch of over 1 million tons per year, as
well as large populations of mackerel, squid, pelagic crabs and certain
other organisms, organization of production of which could increase the
catch in this region to at least 2.5-3.0 'lO" t.

South Pacific. The oceanographic mode, peculiarities of the
composition of the commercial fauna and its distribution in the
southeast Pacific are determined to a great extent by the influence of
the cold Humboldt current and the Peruvian coastal upwelling. Here we
find one of the most numerous fish populations in the World Ocean--The
Peruvian anchovy, which has yielded in certain years, catches of as

391

great as 11-13 million tons, i.e., up to 7,200 kg/km^. This level of
fish productivity is the highest in the World Ocean. In addition to the
anchovies, the pelagic zone is inhabited by tuna, marl in, sauries and
squid. Within the limits of the narrow continental shelf are many hake,
horse mackerel and mackerel, fishing for which could yield over 1
million tons.

The Southwest Pacific is somewhat different, being populated by
such species as sardines, Beryci formes, poutassou, plaice, etc., which
make up over half of the still small catch of the region (0.4«10° t).
The production here is as yet the least of all regions of the Pacific
ocean--only 12 kg/km . Doubtless, the development of fishing in this
region, the resources of which are still negligibly used, will allow an
increase in the total catch to at least 2 million tons, increasing the
useful fish productivity by many times.

The southernmost regions of the Pacific are in the Antarctic.
Here, great resources of Antarctic krill, Serebryanka, etc. wait to be
used.

Indian Ocean. Here, only 2. 7-3. 0*10" t of seafood is caught, 35-40
kg/km'^ for the entire ocean. This is significantly less than the other
ocean basins. Doubtless, one reason is the insufficiently developed
fishing industry, particularly of pelagic fish, but it is thought by
most researchers that even significant intensification of fishing, bring
the catch up to the maximum possible level of 5-6 million tons, would
not increase the fish productivity of the shelf to over 350 kg/km^, of
the coastal pelagic zone to over 250 kg/km^. The most productive
regions are the coastal zones of the northwestern portion of the ocean,
particularly the Gulf of Aden and Bay of Bengal, the waters of the east
African coast, the regions of Madagascar and the Seychelles Islands, as
well as the open regions of the ocean in the areas where masses of water
of different origins come into mingle.

Species fished for here include sardines, large and small tuna,
mackerel, sharks, as well as Sciaenidae, Lucyanidae and other benthic
fish. There are many squids and lobsters (off the coast of Africa),
shrimp and other commercial invertebrates. In the regions around the
subantarctic, there are several species of fish (nototheniids, etc.)
which may be of limited significance. Further development of fishing
should primarily follow the path of utilization of the fish resources of
the pelagic zone, particularly the sardines, mackerel, small tuna,
squid, etc., and also organization of fishing for bottom-dwelling fish
off the west coast of Australia and the east coast of Africa.

To complete our review of the distribution of oceanic commercial
biologic resources, we should emphasize once more that fishing industry
studies of the World Ocean indicate that there is a genuine possibility
of significantly increasing the current catch of ocean fish and large
invertebrates. Catches can be increased to the greatest extent in the
Atlantic (by 10-12 million tons) and Pacific (by 12-14 million tons)
basins. The greatest portion of the probable increase (21 million
tons--87%) will be accounted for by inhabitants of the pelagic zone.

392

Marine mammals (whales and seals) can provide no increase in the current
catch level, and for the next few years, hunting of these mammals will
continue to decrease.

1.4 Basic Trends in Further Development of Ocean Fishing

The study of the processes of biological productivity occurring in
relatively small seas (the Azov Sea, Caspian Sea, Black Sea, Baltic Sea
and North Sea) have shown that the total production of fish (expressed
as weight) is usually 50-100 times less than the annual production of
invertebrate, plankton and benthos. The production of the most valuable
species from the standpoint of food--the tuna, marlin, mackerel,
sail fish, etc., as well as the sharks--which occupy the fourth, fifth or
even sixth trophic levels, are hundreds or thousands of times less than
the production of phytophagous and planktonophagous fish. Thus, based
on the primary production of the ocean, as a result of the tremendous
losses in the intermediate links of the food chain, only a relatively
small quantity of fish production needed for man is created. This type
of loss occurs, in particular, due to the great number of "food
deadends." For example, in the North Sea, over 90% of all of the edible
animals are consumed without any benefit from the standpoint of
commercially valuable animals.

The predominant portion (75%) of Black Sea zooplankton consists of
predators--Sagittae, Ctenophora, Noctiluca, which are almost never used
as food by fish, but they consume tremendous quantities of edible
zooplankton. Losses of this kind are found in the other regions of the
ocean, as well. At best, 30% of the total biomass of the zoobenthos
from the continental shelf of the World Ocean may be used as food by
fish and other commercial species, while the remainder are terminal
links in food chains. Unless a transition is made to commercial
utilization of species at lower trophic levels and significant
adjustments are made to the biologic production processes, we cannot
expect any significant increase in the world catch. One means for
increasing the volume of oceanic biologic resources usable by man might
be the organization of fishing for the massive representatives of
zooplankton. However, in addition to the undoubtable successes, the
first steps in this direction will also involve many difficulties.

Various means and methods of expediently changing individual links
in the oceanic processes of biologic production, making them yield
higher results from the point of view of man, could be of great
significance. Various forms of biologic reclamation, acclimatization
and transplantation of commercial and feed organisms, the creation of
new hybrid forms for stocking of regions with a good food base, but
environmental conditions which are unfavorable for the ordinary species,
incubation and raising of larvae and fry of certain commercial fish, to
be subsequently released in the sea, the creation of "underwater
gardens" and marine fish farms, alteration of the oceanographic modes of
individual regions in the seas and oceans by means of hydraulic
structures, and many other methods should be studied and, possibly, may
be found to be effective for these purposes.

393

A decrease in the quantity of harmful animals by technical,
biologic, chemical or other methods would allow the food resources
available to commercial species to be increased by many times, thereby
facilitating an increase in their population and production. Purposeful
catching of predators might significantly increase the catch of more
peaceful fish. Specialized intensive fishing for a single species (at
times, even a species with no great food value) might open the way for
an increase in the population for another species, the catch of which we
would like to increase. The current scales of commercial effort and the
nature of equipment used for fishing can allow almost complete
elimination of a population. Transplantation of juveniles of commercial
species to more favorable areas for their further growth can improve the
utilization of the food base and yield thousands of tons of additional
fish production. Acclimatization of food and commercial species also
promises to be one method of improving the qualitative composition of
the fauna and increasing the fish productivity of the ocean. Large
areas of the shelf regions of the Barents Sea, Bering Sea, Sea of
Okhotsk and other seas are covered throughout the year by waters of low
temperature, and are far from the wintering areas of commercial
species. They contain over 100 million tons of edible benthos,
practically unutilized by fish. Transplantation of cold-loving
benthophagous fish into these areas might lead to the inclusion of
another, significant food base in the process of creation of fish
production. The great successes of marine "fish husbandry" indicate
that the future for underwater farms, breeding species utilizing the
natural food base, is quite promising.

We should emphasize once more the special significance of the
creation of truly efficient oceanic fish farming for the most effective
utilization of the biologic resources of the ocean and achievement of
the maximum, most stable catch. It should be recalled that the fishing
conducted to date in the World Ocean is far from efficient. We are
seeing cases at the present, for example, of significant changes in the
age composition of stocks under the influence of fishing, leading to a
reduction in the area of distribution, underutilization of the food base
and, thereby, significant reduction in reserves. This is particularly
true of cod in the Arctic-Morwegian area, Atlantic and Pacific sea perch
and many other species. The sharp decline in the population of whales
in the Antarctic has led to underutilization of their food resources
(krill). Naturally, before we take steps to improve the biologic
processes in the ocean, we must develop a plan for efficient utilization
of the biologic resources available with particular caution, carefully
considering the peculiarities of these processes.

All of this requires expansion and deepening of our knowledge
concerning the regularities controlling these processes, the primary
links in the food chain, leading to the final goal--fish productivity,
the energy balance and energy losses during development of biologic
processes and transformation of energy, etc.

The period of prospecting and study of the biologic resources of
the World Ocean is now coming to an end; the time has come to begin the
period of creation of oceanic fish farming; the problem of controlling

394

the biologic processes occurring in the ocean demands solution.

The basic means and methods for further significant increases in

the volume of the seafood catch from the World Ocean are beginning to be

seen; successful employment of these means and methods would allow the
total catch to be at least doubled in the next 20-30 year.

The biologic resources of the World Ocean can and should become the
primary source for satisfying the ever increasing demands of man for
aquatic animals and plants. However, this can be achieved only by
radical alteration of man's attitude toward utilization of the riches of
the sea. In addition to preservation and significant improvement of
traditional fishing, and its transition to a more scientifically
founded, efficient basis, allowing an increase in the present catch to
30-35 million tons and providing some stability for the fishing
industry, the most important methods for future and even greater
increases in total catch must be large-scale development of fishing for
objects at lower trophic levels (particularly krill) and the expenditure
of significant efforts toward the creation of farms for the growth of
aquatic species.

Only by going over to highly productive fish farming in the seas
and oceans, by raising algae, invertebrates, fish, and by actively
increasing the biologic productivity of natural communities, can man
fully utilize the tremendous potential resources of the World Ocean.

395

2. Introduction and Acclimatization of Marine Organisms
(T. S. Rass, 0. G. Reznichenko)

The composition of the fauna and flora of the oceans and seas is
related to a great extent to the history of their formation. Many
regions of the World Ocean are exposed to similar climatic conditions,
but are separated by barriers which are impassable to hydrobionts. The
fauna and flora of these regions contain taxonomically different, but
ecologically similar components, based on vicarious species.

Over the past centuries, and particularly the 20th century, stable
species compositions and relationships of components of biota in many
regions have been disrupted by the introduction (stocking) and
acclimatization of exotic (foreign) species; we shall refer to these
species as exota. The spreading of many species beyond the limits of
their ordinary area of distribution occurs constantly, in spite of the
impediments (in the words of L. A. Zenkevitch), i.e., impassable natural
barriers. The most important means by which hydrobionts are carried
from one body of water to another is man. Independently of the wishes
of man, many species expand their area of development, utilizing
anthropogenic changes in nature: the digging of canals, changes in
estuarine spaces of seas due to decreases and alterations of runoff
resulting from the diversion of water for irrigation, the construction
of dams, the descent of industrial and domestic wastes down rivers, the
dumping of heated water by shoreline power plants. To a still greater
extent, the spreading of exota has been facilitated by transportation.
This is clearly indicated by the fact that, due to the recent spreading
of certain invertebrates carried by ships (the crabs Eriocheir sinensis,
Rhithropnopeus harrisi tridentatus, carcinus maenas, the cirripedia
Elminius modestus, Balanus improvisus, B^. eburneus, the polychaeta
Mercierella enigmatical, the total area of their potential distribution
has now reached 2.5 'lO*^ km^, equal to the total surface of the Barents
Sea, the Baltic Sea, the White Sea and all of the southern seas of the
USSR (Reznichenko, 1976). The naturalization of such autoimmi grants is
greatly facilitated by underwater substrates created by man. Their
total surface is now at least 2,000 km^ (Reznichenko, 1976). Finally,
man actively distributes organisms for their maintenance in aquariums
(from which they frequently enter natural bodies of water) and for
acclimatization, breeding and culturation in new regions.

In connection with the improvement of transportation, the
possibilities of introduction and acclimatization of marine exota have
greatly increased and have become at the present time an important
problem for oceanography. Until quite recently, even the most complete
reviews of oceanography did not even touch on this problem; now, that
would be a clear omission.

396

Factors and Phases of Acclimatization

The possibility of entry of a foreign organism into the composition
of biota formerly foreign to it results from two factors--enclogenous and
exogenous. The endogenous factor is the genuine capability of the
incoming organism to exist in the new body of water, determined by the
agreement of the abiotic characteristics of the body of water with those
required by the exota. Of decisive significance is the presence of
conditions necessary for the most labile period of the life cycle:
spawning and the initial stages of development. The exogenous factor is
the possibility of a species occupying an ecologic niche in a new body
of water by expelling a local species with an analogous ecologic
profile, or by moving into an unoccupied ecologic niche which
corresponds to the ecologic valence of the intruder. Obviously,
addition to endogenous (essentially autoecologic) and exogenous
(synecologic) factors, the geographic factor is also important:
total correspondences of the conditions in the recipient water to the
conditions in the donor body of water, or the primary area of
distribution.

in

the

■■hases of acclimatization during introduction of
i hydrobiont into a new body of water (according
to Zinkevitch, 1940, altered): I-VIII, Phases
of acclimatization; 1-5, Periods of
acclimatization.

Anthropogenic transplantation and introduction of exota into new
bodies of water is performed by man either intentionally
(transplantation) or when these organisms use human transportation
equipment without human intention (autotransplantation) . During
acclimatization in the recipient body of water, in most cases the exota
encounter significant resistance from the local biota, or insufficient
agreement of abiotic conditions to the specific conditions necessary for
life of the transplanted species.

In case of successful introduction of
phases of acclimatization occur (Zenkevitch
phase of barely noticed appearance (due to
intruder, there is usually a phase of rapid
the fact that the intruding species has no
competitors in the new body of water, provi
sufficient. In certain cases, the rate of
be compared to an ecologic explosion (Elton
massive increase in the population of the i

an intruding organism, eight
, 1940). After the first
the small population) of the
multiplication, a result of
natural enemies or serious
ding the quantity of food is
this initial development may
1960). As a result of the
ntruding species, saturation

397

of the new area occurs, the breeding rate of the intruder decreases
(Phase III of acclimatization). For some time the population of this
species remains at the same high level (IV). Then, a phase of slight
(V), and then more rapid (VI) population decrease occurs, due to the
appearance of competitors and natural enemies and a reduction of the
available natural food. Subsequently, the rate of decline slows (VII),
and, finally, the population of the species reaches a certain steady
level, subject to the fluctuations which are normal for all species
(Phase VIII). This detailed system of L. A. Zenkevitch, which reflects
the process of acclimatization quite well, can be reduced to five main
periods (see figure): l--the initial phase--the moment of introduction
(Phase I), 2--the increase in population or intensity of intrusion
(Phase II), 3--the period of high population (Phases III-IV), 4--the
period of decreasing population (Phases V-VII), and 5--the period of
naturalization of the introduced species and the stabilization of its
population (Phase VIII).

2.2 Forms of Acclimatization

Acclimatization of exota can significantly influence the
composition and productivity of the biota of the recipient body of
water. The hydrobionts introduced frequently replace or reduce the
population of local forms. The introduction of the Indian-Western
Pacific diatom Biddulfia sinensis, carried by the hulls of ships, into
the North Sea around 1903, led to its colossal multiplication, and in
some parts of the sea it became the dominant species of phytoplankton
(Hardy, 1956). A gastropod mollusk Crepidula fornicata was
unintentionally carried from the east coast of North America to the
coastal waters of western Europe, where it spread from Sweden to France
(Walne, 1956; Walford, Wicklund, 1973) and became a very numerous
species on the oyster bars, causing significant deterioration in the
conditions of existence of oysters and requiring that the oyster bars be
cleared with special dredges. The boring mollusk Ocenebra japonica,
unintentionally introduced along with the Pacific oysters brought in
from Japan, has done great harm to oysters along the west coast of North
America. Similar occurrences have been reported in the Black Sea, where
the predaceous mollusk Rapana venosa, accidentally brought in from the
Sea of Japan, has acclimatized and has virtually wiped out all of the
oyster bars in the eastern portion of the sea in a few years, greatly
reducing the biomass of other large bivalve mollusks.

We must distinguish substitution acclimatization, such as the cases
we have just described, from interstitial acclimatization (a term used
by Zenkevitch, 1963), when the new species inserts itself into the
composition of biota without any apparent expulsion of any aboriginal
species. Examples of interstitial acclimatiztion are rather obvious in
cases of intrusion of species which differ in terms of ecology from the
components of the biota of the recipient body of water. For example,
the planned introduction of the polychaete worm Nereis di versicolor, the
bivalve mollusk Abra (=Syndesmya) ovata and the mullets^Liza (=Mugil)
aurata and _L. sal i ens from the Azov Sea to the Caspian Sea in 1938-1947
has led to a significant increase in the biomass of the benthos of the
Caspian Sea and to the formation of a Caspian population of mullets.

398

apparently nearly as numerous as the initial population. In this case,
expulsion of local forms was not observed, and the acclimatization was
doubtless useful from the practical point of view. A similar result was
obtained by the carefully planned and well-founded introduction of
certain reef and estuarine species of fish and invertebrates to the
Hawaiian Islands. The Hawaiian Islands are poor in natural fauna, as is
the usual case for isolated islands, the local fauna consisting mainly
of species which have a long larval period, so that larvae can be
carried in by currents from the life-rich regions of the tropical
western Pacific. The islands had no representatives of the species-rich
genera of fish Lutianus and Lethrinus, had only 2 species of groupers
(Epinephelus) and 2 species of the ITTupeid group of sardines, of which
other islands in Oceania had from 8 to 22 species. The mollusks and
crustacean fauna were similarly poor. As a result of transplantation
from the waters of the Atlantic states of America, the islands of
central Oceania, Japan and Southeast Asia, the marine fauna of the
Hawaiian Islands was enriched with useful mollusks, crustaceans and
fish, which acclimatized with no noticeable harm to the local biota
(Table 20).

The relative level of saturation of biota is of great significance
for the introduction and acclimatization of exota, since it defines to a
great extent the possible direction of introduction and form of
acclimatization. This is well illustrated by comparison of the fauna of
bodies of water which are more or less similar in their physical and
geographic conditions but differ in terms of saturation of biota.

For example, joining of the Mediterranean and Red Seas through the
Suez Canal in 1869 opened a path for the fauna of these bodies of water
through what had been an impassable barrier. There are difficulties in
this method--highly saline water areas (Great Salt Lake, etc.).
Nevertheless, some 130 species from various systematic groups of benthos
and nekton have succeeded in using such opportunities to introduce
themselves into new bodies of water. Eighty-five species of
invertebrates and 25 species of fish from the Red Sea have settled in
the Mediterranean, while 6 species of invertebrates and 7 of fish from
the Mediterranean have settled in the Red Sea (Table 21). The
difference in the number of fish moving in the two directions has
resulted from the fact that the fauna of the Mediterranean Sea
represents significantly fewer species than the Indian-Western Pacific
Ocean fauna. For example, in the Mediterranean we find no species of a
number of characteristic Pacific families: Dussumieridae (2 species
have settled in the Mediterranean), Platycephalidae (1), Siganidae (2),
Leiognathidae (1 species).

2 . 3 Transoceanic and Inter-oceanic Transplantation

The global scale which has been achieved by transplantation and
introduction of marine organisms is illustrated by examples of both
autotransplantation and of transplantation. Long-range autotrans-
plantation of invertebrates is clearly seen in examples of
transplantation by ships, on their hulls or in ballast water (Bishop,
1951; Walford, Wicklund, 1973; Hoese, 1973, et al.). We can present

399

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400

Table 21. Autointroduction from the Suez Canal of various hydrobionts
(according to Walford and Wicklund, 1973).

Number of Species

Group

Passing from Red Sea

From

Mediterranean

to Mediterranean

to Red Sea

1

2

2

3

29

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10

2

14

1

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16

Algae
Sponges
Coelenterata
Worms (Polychaeta,

Sipunculoida)
Crustacea
Pantopoda
Molluska
Echinodermata
Ascidia
Fish
Total

examples of transplantation of 5 species of the Cirripedia crustaceans,
the Balanidae, attached to the hulls of ships: from Australia to the
waters of western Europe (Elminius modestus, about 1940); from the coast
of America to the coast of Europe, southern Australia and Japan (Balanus
improvisus, late 19th and early 20th centuries), from the Atlantic coast
of America to Europe, then later to Japan (B^. algicola); from the
tropical Pacific to Japan and California (B^. amphi trite, about 1940 and
later). Autotransplantation of other invertebrates overgrowing the
hulls of ships has occurred over equally long distances: the polychaete
Hydroides norvegica, the Bryozoa Bugula flagellata, the hydroid
Bougainvfllia ramos"a--from the North Atlantic to Australia and New
Zealand; the polychaete Mercierella enigmatica--from India to western
Europe and the Caspian, the Bryozoa Victorella pavida--in the reverse
direction. Ships have also carried many other species across oceans
which have acclimatized in new regions: the mussels Mytilus edulis--
from Europe to Japan, the North Atlantic Mya arenaria to the Pacific
waters of America and to the Black Sea, the Rapana venosa from the Sea
of Japan to the Black Sea, the crabs Callinectes sapidus and
Rhithropanopeus harrisii tridentatus from the waters of eastern North
America to the seas of Europe, and the last-named species also into the
Caspian Sea and the Pacific waters of America; the European Carcinus
maenas--to the Atlantic waters of America; the East Asian Eriocheir
sinensis--to the waters of western Europe. Cases are known of
transoceanic autotransplantation of fish--small bullheads, blennies,
etc. --in the ballast water of ships, during transportation of dry docks,
shipping of large mollusks, etc.

401

Acclimatization by means of planned or sporadic transoceanic
shipment has been performed on a particularly large scale for oysters
and fish. At various times, 7 species of oysters have been
transplanted. Successful transoceanic naturalization has been achieved
for only some of them. For example, the European oyster Ostrea edulis
has been acclimatized off the Atlantic coast of America, off the shores
of South Africa and in Japan. The Virgin Islands oyster Crassostrea
virginica has been naturalized along the Pacific coast of America and in
Hawaii, where it was taken from California. The Pacific oyster C^. gigas
has been acclimatized along the east coast of America, in Hawaii,
France, Australia and New Zealand. As concerns the remaining species of
oysters, their introduction in regions not as far from their natural
area of distribution has been partially successful. The practical
significance of the acclimatized oysters has been very great: the
oysters acclimatized in new regions have yielded significant
production. For example, the annual production of the far-eastern
oyster in the western waters of America is 30-40*10"^ t.

Transoceanic introduction and acclimatization of marine commercial
fish is, actually, of significant practical interest. These operations
have been performed, however, primarily with transitional (anadromous)
and semi transitional species, and only to a smaller extent with true sea
fish. One significant achievement has been the introduction of the
anadromous Alosa sapidisima from the Atlantic coast of America to the
waters of the Pacific coast, achieved by the transportation of
developing eggs in 1871-1886. This shad was naturalized in 1873, and by
1886 had become one of the most numerous commercial fish in
California. It extended to the north and south from its point of
introduction, occupying an area of distribution from Mexico to Alaska (a
few even reaching northeast Asia). The greatest catch, about 3,000
tons, was achieved in 1914, after which the catch decreased to 300-1,000
tons per year (Mansueti, Colb, 1953; Walford, Wicklund, 1973).

In 1879 and 1882, fry of the semi transient Roccus saxatilis
(frequently improperly called striped perch) was transported from the
Atlantic coast of the USA and released in San Francisco Bay. This fish
was naturalized in the waters of the Pacific, occupying an area of
distribution from British Columbia to southern California and yielding
commercial catches of up to 500 tons per year (Raney, 1952).

Beginning in 1872, many attempts have been made at transoceanic
transplantation of salmon, particularly species of the Pacific genus
Oncorhynchus. Attempts have been made to introduce Pacific salmon to
various regions of the Atlantic Ocean, from Canada to Florida and from
Norway to Italy, in Mexico, Nicaragua, Hawaii, Argentina, Chile,
Australia and New Zealand (Davidson, Hutchinson, 1938). The Pacific
salmon have acclimatized (Stokell, 1955; Rodway, 1957) in a few regions
of northeast America (silver and humpback salmon in the rivers of the
Gulf of Maine, New Brunswick and Ontario), in Chile (silver salmon,
blue-back salmon), and the south island of New Zealand (king salmon,
blue-back salmon). However, the populations formed in the regions have
frequently gone over from an anadromous to a river mode of life, as a
result of which their population has been greatly reduced (Stokell,

402

result of which their population has been greatly reduced (Stokell,
1961) or even completely eliminated (in the Gulf of Maine). In 1933-
1939, in the Soviet Union, dog salmon were introduced to the rivers of
the White and Barents Seas, but this experiment was not successful. In
1956-1964, each year, developing eggs of humpback salmon, and, in
smaller quantities, dog salmon, were transported from Sakhalin to Murman
and the White Sea, where the eggs were reincubated, the larvae and fry
were released into the sea. In all, some 49 million individuals were
released. In 1960, humpback salmon, apparently some of those fry
released in 1959, returned to the coast of the White Sea, Murman, as
well as Norway, England, and Iceland; in all, over 80,000 individuals
were counted (Shearer, 1961). Later, great runs of humpback salmon were
reported in 1965, 1971 and 1973, while in the other years, the runs were
much smaller--a few dozen to a few thousand fish. Since 1966, stocking
of fry has been resumed. Apparently, complete naturalization of the
humpback salmon to the European north has not occurred, and its
existence there is supported by the transport of eggs from Sakhalin and
maintained by the fortune of favorable weather conditions (mild winters)
in some years.

Transplantation of commercial sea fish in the Pacific Ocean basin
has involved as yet only a few species. The natural area of
distribution of the valuable milkfish (Chanos chanos) a hundred years
ago encompassed the indo-west Pacific and extended from the Red Sea and
east Africa to Hawaii and Polynesia. In 1876-1877, a small number of
chanos larvae was released in the sea near San Francisco (H. M. Smith,
1896). Finding a free ecologic niche and favorable conditions there,
the chanos was fully naturalized and spread south--into the Gulf of
California (McHugh, Fitch, 1951) and along the coast of Central America
to Panama. At the present time, the milkfish is one of the commercial
species of fish along the Pacific coast of Mexico (Berdegue, 1956;
Schuster, 1960; Lachner et al . , 1970). The successful introduction of 4
species of sea fish from the Society Islands and the Marquesas to the
waters of Hawaii was described earlier. We should also recall the
successful acclimatization of the salt-water tilapia (Tilapia
mossambica) to estuaries, after it was transported to Honolulu from
Singapore in 1951.

The introduction of 2 species of mullet from the Black Sea into the
Caspian Sea was quite successful. The prospects for the introduction of
the temperate and cold-water far eastern Kamchatka mackerel
(Pleurogrammus monopterygius) into the Barents Sea are quite good. A
small number of developing mackerel eggs was successfully transplanted
to eastern Murman in 1958, 1971-1972 and 1976, where they incubated and
the viable larvae were released into the sea (Rass, 1962, 1965). This
work has, unfortunately, remained uncompleted.

The transplantation of organisms desirable to man is, in many
cases, accompanied by unintentional autointroduction of undesirable
animals, due to insufficient caution in the selection of materials.

403

2.4 Parameters of Introduction and Acclimatization of Exota.

The actual possibility of introduction and acclimatization
(naturalization) of exota is determined by the physical-geographic,
autoecologicand synecologic, or biotic parameters. The possibility of
acclimatization is determined primarily by the agreement of the
physical -geographic (abiotic) conditions of the acceptor body of water
with the conditions in the donor body of water. The basis of this
agreement in naturally separated regions is the symmetry of the ocean
(Zenkevitch, 1948). Regions of the oceans which are located in areas of
similar climate but are separated by impassable continents, climatic or
water barriers, may be quite similar in terms of abiotic conditions.
The regions of the Boreal labitudes of the Atlantic and Pacific Oceans,
the western and eastern waters of these oceans, the Boreal and Notal
regions, the Arctic and Antarctic, as well as the tropical areas of the
Atlantic, Indian and Pacific Oceans are comparable in this aspect. The
capability for acclimatization and naturalization is determined by the
autoecologic parameters when the acceptor body of water has the
conditions necessary to the intruder species during the period of
reproduction for survival of the eggs and larvae, which are more
vulnerable than the species in other periods of life. The possibility
of introducing exota is determined by synecologic parameters, depending
on the local biota, the existence of an ecologic niche which is open, or
occupied by a less viable local species, the presence of sufficient food
resources, the resistence of the intruder in terms of parasitic invasion
and its susceptibility to local predators. These parameters basically
determine the nature of acclimatization, either interstitial or
replacement (Zinkevitch, 1963).

The presence of an unoccupied niche in the biota of individual
regions of the ocean is determined by the geologic history of the fauna
and flora. Quite demonstrative in this respect, for example, are the
unoccupied or weakly occupied niches of the southern Boreal transitional
fish off the Pacific coast of North America (in comparison to the
Atlantic coast), the niche of silt-feeders in the Caspian (in comparison
to the Azov Sea), the niche of temperate and cold-water fish in the
Barents Sea (in comparison to the Bering Sea), the niches of a number of
tropical species in Hawaii and the eastern Mediterranean, of brackish-
water hydrobionts in the Caspian Sea, Boreal fish in the cool layer of
water at 50-100 m depth in the Black Sea (in comparison to the Baltic
Sea), the niche of the tropical phytoplanktophages in the Caribbean Sea
(in comparison to the South China Sea and, after acclimatization of the
chanos, to the Pacific waters of Mexico), the niche of large
benthophages in the Arctic (in comparison to the Antarctic), etc. These
niches are easily filled by immigrants from more life-saturated regions,
or may be filled by introduction of the corresponding species (Rass,
1965, 1975).

Unoccupied niches in the seas are also created as a result of human
activity, which may change the environment and the composition of biota
by changing the mode of continental runoff, resulting in a decrease in
the population of transitional fish, or by extremely selective fishing
for certain fish, as well as development of their competitors. The

404

niches thus liberated can be filled, for example, in our own southern
seas, by the introduction of sea fish: the Baltic herring and the Black
Sea anchovy and garfish to the Caspian Sea, the Japanese pike-perch to
the Black Sea (Rass, 1965, 1975). The unoccupied niches are easily
filled by autointroduction of undesirable, useless or even harmful
species, utilizing human technology. Therefore, it is important not to
delay introduction, efficient transplantation and acclimatization of
desirable commercial and food organisms needed by man.

405

CHAPTER II. EFFECT OF OCEAN POLLUTION
ON MARINE ORGANISMS AND COMMUNITIES

1. Chemical Pollution and Its Effect on Hydrobionts.
(S. A. Patin)

The effect of man on the living resources of the biosphere,
including the World Ocean, is not limited to simple extraction of
biologic production, cultivation and alteration of the composition and
structure of populations. Over the last few decades, the influence of
industrialization and urbanization of modern society, intensification
and increased use of chemicals in agriculture and other attributes of
scientific and technical progress have particularly rapidly grown and
expanded, resulting in pollution of the biosphere and the appearance of
new ecologic factors. The environment is being transformed to a
qualitatively new state, which is sometimes referred to as the
"biotechnosphere" (Khil'mi, 1975).

The pollution of the World Ocean occupies a special place in the
framework of this complex and multifaceted problem. Many, if not most,
of the toxic substances liberated by man on land enter the ocean,
creating situations of local, regional or global pollution of the seas
and oceans. Due to the unity of the structure of the ocean, regional
anomalies are reflected in the status of neighboring regions and of the
entire system as a whole.

As a result of pollution, the distribution of certain artificial
substances has become planetary. The material chemical composition of
the marine environment, formed over the duration of a number of geologic
eras, to which the animal and plant life of the seas and oceans has
adapted by evolution, is undergoing noticeable, at times significant,
changes in the space of decades. The biologic consequences of this
process, involving the formation of a new quality of the marine
environment, cannot but attract the attention of modern science and must
be the subject of comprehensive study in many nations of the world. The
status and results of this type of work go far toward determining the
nature, scale and effectiveness of national and international efforts to
protect the seas and oceans from pollution.

1 . 1 Status and Methodology of Investigations.

We can distinguish three main trends in the overall system of
ecologic studies on the problem of pollution of the World Ocean:

- Pollution monitoring--a system of observation, testing,
estimation and prediction of the quality of marine environment;

406

- Biogeochemistry of pollutants-- the study of the elements of
balance, processes of biologic concentration and transport through the
food chain, biogenic migration and transformation of artificial
substances in marine communities and ecosystems;

- Ecologic toxicology--the study of the effects of toxic factors on
the hydrobionts and communities, estimation of the biologic and ecologic
consequences of the pollution of the marine environment, regulation of
permissible norms for the content of toxic substances.

The level of development of the basic principles and methodology of
studies in each of these three areas differs significantly. Studies of
situations of pollution of individual marine regions are most
advanced. This has been facilitated by the successes achieved in
processing large volumes of information and the progress in the area of
analytic methods of detection and recording of trace quantities of man-
made substances in natural environments and substrates. The
methodologic principles of large-scale monitoring are being intensively
developed in our country and abroad, and also by means of international
cooperation (Goldberg, 1970; Marine Environmental Quality, 1971).

The situation is quite different in the area of marine
biogeochemistry of toxicants and ecologic toxicology. In spite of the
abundance of the works dedicated to various aspects of the interaction
of marine organisms and communities with toxic man-made components of
the environment, the general methodology of studies of this nature, the
foundation of areas for study and summarization of the available
materials are essentially in the earliest stages of development. This
is particularly true of marine ecotoxicology--a new area of ecologic
investigation at the junction of marine biology, toxicology and
experimental ecology.

It should be noted that marine ecotoxicology and the
biogeochemistry of pollutants mutually supplement each other, studying
two aspects of a single process of interaction between marine organisms
and the anthropogenically altered toxic environment. The situation is
somewhat similar in the area of study of radioecologic phenomena in the
ocean (Polikarpov, 1964).

In terms of methodology, it is important to emphasize that
ecologic-toxicologic studies should be directed toward the study of
anomalies in marine communities and ecosystems under conditions as close
to natural conditions as possible. Studies performed directly in
polluted regions are ideal from this standpoint (Bechtel, Copeland,
1970; Bellan, Bellan-Santini , 1972; Mironov, 1972; Nelson-Smith, 1973);
however, they are possible only in cases of actual severe pollution,
when the biologic effects are obvious and can be directly quantitatively
measured. It is much more difficult to evaluate the actual or
potentially possible results under conditions of low levels of chemical
pollution. In these situations, the methods of experimental ecology,
toxicology of representative species and communities of marine
organisms, estimation of their production in situ in the presence of
toxicants, experimental modelling of food chains and ecosystems, and a

407

number of other methodologic approaches must be used (Patin, 1971;
Fontaine, 1972; Aubert, 1973; Patin et al., 1975).

1.2 Basic Features and Trends in Pollution of Ecologic Zones of
the World Ocean.

The flow of publications on the problem of chemical pollution of
the marine environment and hydrobionts in recent years has greatly
expanded and amounts to some thousands of articles; however, summary
works are rare (Goldberg, 1970, Marine Environmental Quality, 1971;
Mironov, 1972; Aubert, 1973; Nelson-Smith, 1973; Loranskiy et al . ,
1975). In particular, we know of no description of the most general
regularities of the process of pollution of the seas and oceans in
relationship to the specifics of the biologic structure and biologic
production in the World Ocean.

One interesting but as yet unrealized approach to the analysis of
the large-scale picture of distribution of man-made chemical products in
the ocean is the utilization of the extensive materials available on the
behavior and transfer of artificial radionuclides in the biosphere. If
we consider that the large-scale (background) pollution of the biosphere
is determined primarily by atmospheric transfer and fall-out of
pollutants from the atmosphere, it is difficult to find any other
precedent involving large-scale pollution of the biosphere in which
these processes would be more clearly and obviously reflected than in
the cases of distribution of the products of nuclear testing. The great
magnitude, scale and variety of studies on this problem, including
studies concerning artificial radioactivity of the marine environment
and organisms, are also without precedent.

The existence of an atmospheric reservoir for the primary groups of
chemical toxicants and the magnitudes of the flows of these toxicants
into the World Ocean can be judged from the information presented in
Table 1, from which we can see that, with the exception of crude oil,
all of the polluting substances enter the World Ocean to a great extent
through the atmosphere.

Each year, some S-IO^ t of fossil fuel is burned in the world, and
over lo" t of solid, vapor and gaseous compounds are emitted into the
atmosphere (Styrikovich, 1975). The existence of large-sale atmospheric
transfer of man-made substances from the land into the ocean is
indicated by the discovery of ash particles in the bottom sediment of
the open ocean and the accumulation of heavy metals in the glaciers of
Greenland (Bertine, Goldberg, 1971).

Atmospheric aerosols and fall-out over the ocean have been found to
contain significant quantities of such products as DDT, polychlorinated
bi phenyls, mercury, lead, ash, in particles on the order of 1 m in
diameter, about the same size as the aerosol particles of radioactive
fission products, meaning that they can be carried by the atmosphere
over long distances from their source and can reach the upper layers of
the atmosphere.

408

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In addition to the generally known groups of large-scale toxicants
(petroleum and its products, heavy metals, chlorinated organic
compounds), we should mention two more types of substances, the
liberation of which into the environment is quite extensive. We are
speaking of volatile organic liquids and gases (dichloroethane, freons,
solvents) and carcinogenic substnces, which have blastomogenic
properties (polycyclic aromatic hydrocarbons such as benzpyrene).
information on the content of such substances in the sea and its
orgnisms is as yet sparse; however, the scale of their production and
entry into the environment is quite large: the annual rate of
liberation of dichloroethane and freons into the atmosphere is at least
1 million tons, of volatile organic solvents up to 2 million tons
(Marine Environmental Quality, 1971). The total quantity of persistent
anthropogenic hydrocarbons (in addition to methane) entering the
atmosphere is about 50 million tons per year (Duce et al . , 1974). To
this figure we must add the pollution of neritic marine waters and of
the open ocean by solid wastes, consisting of various insoluble plastics
and organic films, the world production of which is over 20 million tons
per year (Marine Environmental Quality, 1971). A significant fraction
of these products finally reaches the ocean. For example, the mean
content of plastic particles in the Sargasso Sea is 290 g/km
(Carpenter, Smith, 1972).

We also must not forget the processes of eutrophication resulting
from the liberation of organic substances, fertilizers, detergents and
other compounds of phosphorus and nitrogen, leading to the intensive
development of phytoplankton and certain species of benthic algae and,
thus, to secondary pollution of the sea with the products of their
metabolism and decay. However, these processes, like the processes of
thermal pollution (see Chapter II, 3.), are generally localized in the
neritic waters or internal bodies of water, and should not be considered
to be a global situation.

Let us attempt briefly to describe the basic structural and dynamic
peculiarities of the field of large-scale pollution of the ocean.

Increased pollution of the euphotic layer. --This distribution
feature is rather obvious, since it is the surface waters which are the
primary collectors of atmospheric pollution, littoral runoff, sewage and
wastes of the most varied composition and origin. Depending on the rate
of exchange and renewal of surface waters and, at times, on the rate of
biosedimentation processes (Patin, 1970), a certain gradient of vertical
distribution of pollution is created in the water; however, the levels
of content of toxicants of all kinds generally reach their maximum in
the surface layer.

Increased pollution of the neritic zone. --The available data on
pollution of the seas and oceans indicate that there is a gradient of
decreasing concentration upon transition from the neritic zone to the
open ocean, resulting from the delivery of polluting substances into the
sea from the land and their gradual dilution with increasing distance
from the source, the localization of many types of human activity
causing pollution (navigation, drilling for petroleum) in the shallower

410

regions of the ocedn, and the gradual purification of the air by fall-
out of aerosols as they move over the water body. Especially persistent
fields of high levels of regional pollution are created in areas with
limited water exchange, for example in the internal seas.

Zonality of distribution and the latitude effect. --As has been
shown, using radioactive products as an example, finely dispersed
aerosols are transferred and precipitate from the atmosphere in the
zonal direction, forming latitudinal zones of intensive pollution at the
parallels where the sources of atmospheric pollution are located
(Karol', Malakhov, 1965; Nelepo, 1970). As a result, in the temperate
latitudes of the northern, and to a lesser extent of the southern
hemispheres, there are maxima of precipitation and pollution, while at
the equator and in the polar regions there are minima. This global
picture has been produced on the basis of observed data on the
continental surface; however, there is every reason to extrapolate it to
the World Ocean as well.

Atmospheric flux of chemical pollutants is primarily concentrated
in the northern hemisphere, particularly at 30-70°N, where the main
industrial zones are located and where most of the substances are
produced which pollute the troposphere and subsequently precipitate into
the ocean. According to some calculations, some 90% of all atmospheric
pollution is accounted for by these regions (Duce et al., 1974). If we
consider the zonality of the transfer of tropospheric aerosols noted
above and the restriction of the maximum precipitation to the middle
latitudes of the northern hemisphere, we can speak of the existence of a
latitude effect in the large-scale distribution of chemical pollutants
in the ocean with its maximum in the temperate latitudes of the northern
hemisphere (see figure).

These considerations have been confirmed as yet only by the results

of studies of artificial radioactivity (Popov, Patin, 1966), plus some

information on chemical pollution of the waters of the North Atlantic
(Simonov et al ., 1974).

The mosaic nature of distribution. --Analysis of this phenomenon as
applicable to artificial radionuclides has shown (Popov, Patin, 1966)
that it cannot be explained by analytic errors in the determination of
impurities in the sea water alone. This heterogeneity is characteristic
for all trace elements in the marine medium, and its causes are probably
related to the peculiarities of turbulent mixing of masses of water and
the overall specifics of the behavior of trace quantities of substances
in complex heterogeneous systems such as sea water. In this connection,
we must recall the processes of sorption, hydrolysis and complex
formation, which lead to the complicated and "anomalous" behavior of
many tr^ice impurities under conditions of great dilution in aqueous
solutions.

Localization in the surface film. --This feature of the
microstructure of the field of pollution is related to the physical-
chemical and ecologic peculiarities of the thin surface film at the
division boundary between the water and the atmosphere, where many

411

Number of species in thousands

N M° 60° Jff'

ff'

jff° &ff' sff' S

Zonality of distribution of certain biologic characteristics of the World
Ocean and levels of pollution of surface (euphotic) layers of sea \vater.

a--Number of species of marine animals (after L. A. Zenkevitch) ;

b, c--Biomass of benthos and plankton (after B. G. Bogorov and L. A.

Zenkevitch); d--Cumulati ve global store of strontium-90 (Patin, 1965);

e--Hypothetical curve of variation in levels of chemical pollution.

Shaded areas show position of latitude band of elevated pollution.

412

natural organic compounds with hydrophobic and surface-active properties
Are concentrated, creating a unique biotope of neustonic marine
communities (Zaitsev, 1970). The known facts of localization of a
number of toxicants in the surface film (Seba, Corcoran, 1969) have been
confirmed by our own data (Table 2) obtained upon analysis by gas
chromotography and atomic absorption of samples of sea water (film 60-
100 ijm thick).

Table 2. Distribution of certain ingredients between the surface film
and sea water (Arcachon Bay, France, summer of 1973).

Mean concentration, yg/l Coefficient of
Ingredients In surface film In upper level accumulation in
60-100 um thick down to 50 cm surface film

10+1 85

0.10+0.02 950

0.10+0.02 860

0.07+0.02 630

0.10+0.02 1,050

0.5+0.1 550

13.5+3.5 2,200

0.4+0.1 300

0.3+0.1 800

22+4 470

Anionic

detergents

850+75

DDT & DDD

95+10

DDE

86+9

Lindane

44+8

PCB

105+15

Hg

2

,750+110

Pb

2

,920+180

Cd

120+35

Cu

235+15

Zn

1

,020+45

It must be recalled that the organisms of the hyponeuston include

the stage of early ontogenesis of many hydrobionts, including commercial

fish, and that this stage is most sensitive to toxic effects
(Polikarpov, Zaitsev, 1969).

Superimposi tion of fields of pollutants and bioproducti vi ty .--The
general picture of the distribution of biologic productivity in the
World Ocean can be characterized by concentration of living organisms in
the surface layer and particularly in the neritic zone and the internal
seas. It is in these zones also that the main fluxes and masses of all
types of toxicants entering the marine environment are concentrated.
Furthermore, the interfaces between the water and atmosphere, water and
bottom, water and coast, river water and sea water, where complex
physical, chemical and biologic processes occur, determining to a great
extent the life of the ocean, are also areas of localization of higher
concentrations of pollutants.

Relative stability of fluxes and levels of toxicity. --In contrast
to the situation of strong but one-time local pollution, for example in
case of an accident, when the toxicity of the environment, after

413

reaching its maximum, gradually decreases, large-scale pollution not
only does not decrease its intensity as long periods of time pass, but,
in terms of a number of its indices, is gradually increasing. This is
quite understandable if we consider the relative stability and the
increasing trend of the characteristics of world industrial production,
which correlate directly to the fluxes and levels of pollution of the
hydrosphere.

1.3 Biologic and Ecologic Effects of Pollution.

The basic difficulty which arises upon analysis of the effects of
anthropogenic changes in the chemical composition of the marine
environment results from the fact that living systems react to the
presence of toxic or other pollutant ingredients at the same time at all
levels of organization of life--from the subcellular to the
superorganismic. A complex mosaic of direct and indirect mechanisms and
manifestations of the effects of toxicants arises, against the
background of the natural dynamics of biologic processes.

Various versions of systematization of biologic effects and
aftereffects of pollution of the marine environment are possible. In
the first approximation, it is desirable to differentiate two groups of
ecologic-toxicologic situations: direct toxic or stress effects on
separate populations and communities, accompanied by rapid damage to the
primary physiologic-biochemicl systems of organisms, with subsequent
lethal intoxication, elimination of individual species or clear
pathologic changes, and the effect of comparatively low concentrations
of pollutants on the organisms and communities upon long-term, chronic
pollution. The impressive, at times tragic, examples of situations of
the first kind, usually arising as a result of an accident or one-time
spill of industrial wastes, are well known (Fontaine, 1966; Mironov,
1972; Aubert, 1973). Fortunately, these areas of intensive pollution
are usually located within very limited zones in the sea and the results
of such events, even if quite severe, do not extend over broad areas of
water. The second group of effects is not so obvious, and has been much
less studied. Due to differences in the level of resistance of various
species and of various stages of ontogenesis of hydrobionts, a complex
chain of biologic reactions and responses arises in the community, the
final and most significant manifestation of which is a change in the
equilibrium and stability of the community. These changes may be
manifested as a decrease in the index of species variety (Bechtel ,
Copeland, 1970), a disruption in the timing and relationship of
processes of production and destruction of organic matter (Kamshilov,
1968), anomalies of the dynamics of dissolved oxygen (Braginskii, 1972),
changes in dominant species in the biocenosis (Bellan, Bel lan-Santini ,
1972) or other ecologic disruptions (Woodwell, 1970).

The non-obvious nature of this type of result, in comparison to
acute intoxication (for example, massive fish kills) does not mean that
these consequences are any less serious or significant. The situation
is more probably the opposite, considering the scale and universality of
large-scale pollution, as well as its other aspects, noted above
(correlation with distribution of biologic productivity, constancy of

414

levels, etc.); we can assume that large-scale ecologic anomalies are
occurring in the ocean. This aspect has not as yet received its
deserved attention from researchers, although its importance and urgency
for the entire problem of pollution are obvious. In this respect,
processes of biologic productivity in the ocean and, particularly, of
the formation of organic matter under conditions of chronic pollution of
the euphotic zone, should be given particular attention. The problem
here is not only related to the fundamental ecologic significance of
primary production as the material and energetic basis of life in marine
bodies of water, but also the increased vulnerability (sensitivity) of
photosynthesis and the community structure of single-celled algae to
disruptions in the chemical composition of the environment in which they
live. The clearest and best known examples of ecologic anomalies of
this type are cases of eutrophication (or, more precisely, hyper-
eutrophication) of sea water and, particularly, fresh water, as a result
of the entry of large quantities of biogens from the land into the
water.

Less known and not so well studied are examples of inhibition of
growth, development and photosynthesis of marine phytoplankton as a
result of the content of various toxicants or their combinations in sea
water. Table 3 presents summarized ecologic-toxicologic information on
the effects of toxicants on cultures and natural communities of marine
phytoplankton. As we compare the orders of magnitude presented in Table
3 (greater accuracy is impossible, since we are speaking of general
features of a complex and dynamic system), it is easy to see that in
spite of the great variability, the levels of threshold toxicity of the
substances in question for phytoplankton overlap the range of the
content of these same substances in the neritic zone, and for some
toxicants (petroleum products, polychlorinated biphenyls)--the oceanic
zone as well. In other words, the presently existing and repeatedly
recorded concentrations of the most common man-made products in sea
water are capable of altering the rates of formation of organic matter
in the World Ocean.

The extrapolation of experimental data to natural ecosystems which
lies at the basis of this conclusion is, naturally, based on certain
assumptions. However, if we consider that some of the data in question
were obtained under conditions in situ and in long-term experiments, and
that there is direct proof of disruptions of the production and
structural characteristics of marine phytoplankton in anthropogenically
changed environments (Clutter, 1970; Kiryushina et al . , 1975;
Oradovskii, 1975; Patin, Ibragim, 1975), the idea of large-scale
inhibition of photosynthesis, at least in the most polluted regions of
the neritic zone of the World Ocean is, in our opinion, well founded.
The question of the ecologic results of a large-scale inhibition of
photosynthesis in the World Ocean is worthy of special study. For
example, a large-scale decrease in primary production by 10%, which
hardly seems excessive to us, given today's level of pollution, should
result in a corresponding decrease in the rate of production at other
trophic levels, right up to the nekton, where these losses would amount
to tens of millions of tons, including several millions of tons of
commercial fish, each year.

415

Table 3. Natural, anthropogenic and toxic (for phytoplankton) levels of
the content of chemical ingredients in the euphotic layer of the marine
environment, ng/1 .

Anthropogenic levels
Ingredients Natural Oceanic Neritic Threshold

levels zone zone toxicity level*

Dissolved petroleum

products - lO^-lO^ 102-10^ lO^-lO^

Heavy metals o i o i i

Mercury IQ-'^-lO-^ >10-'^ lO'l-lO IQ-^-lO

Lead IQ-^-l IQ-l-l loO-lO^lO^-

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Chlorinated
hydrocarbons

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Polychlorinated

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10-1-10

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Aliphatic

hydrocarbons - 10--^-10-^ ? ?

DDT and its

metabolites - <10-2 10 10-1-10

*Minimum concentration of toxicants in the environment at which
significant (usually 50% inhibition of photosynthesis or of cell
division of phytoplankton has been observed.

Among the probable anthropogenic modifications of the normal course
of hydrobiologic processes in the ocean, which have never been studied,
we must also include such phenomena as disruption of the complex system
of external metabolic interactions in communities of marine organisms.
The exchange of metabolites among organisms, with the high intensity
inherent in it and the biochemical specificity of synthesis and
consumption of metabolites, plays an extremely important role as an
integrating and regulating factor in marine communities (Khailov,
1971). It is not difficult to imagine that even low concentrations of
pollutants foreign for the biotope (for example, dissolved petroleum
products) could block various metabolic interactions of the organisms
and thereby disrupt the system of biologic communication in communities
and, consequently, their structural and production characteristics. The
same is probably true as concerns sensory connections of hydrobionts,
their ethologic reactions, chemoreceptions and other phenomena, the
mechanism of which may be disrupted if small quantities of man-made
impurities are present. Due to the complexity and "veiled" nature of
such effects, little is known of them, but still, observed facts, such
as disruptions in the migrations of fish caused by pollution, indicate
that such ecologic anomalies are quite real.

416

Another group of "critical" situations in marine communities is
related to the phenomenon of concentration of toxic microimpurities at
the boundary between the water and the atmosphere and between the water
and the bottom, which we mentioned earlier, and the influence of
toxicants on the most vulnerable organisms and communities of the
neuston and benthos. Whereas the reactions of the marine benthos to
toxic factors have been rather widely studied, particularly in areas of
high pollution (Bellan, Bellan-Santini, 1972) and in acute-toxicity
experiments (Stora, 1974), the neuston has as yet fallen outside the
sphere of marine ecologic-toxicologic studies, although its
vulnerability to the influence of toxic factors is known (Polikarpov,
Zaitsev, 1969). This opinion is reinforced by many reports concerning
increased sensitivity of the early stages of development of marine
organisms, many of which pass through a neustonic phase of life and are
subject to severe toxic and even mechanical effects resulting from
pollutants located in the biotope of the neuston during this period of
their life. For example, even such a common phenomenon as a thin film
of oil on the surface of the sea can cause the death of the larvae of
physostomous fishes, which it isolates from the atmosphere, preventing
filling of the swim bladder with air (Vinogradov, 1972).

There are other ecologic situations and aspects of this problem,
for example the accumulation and migration of toxicants through the food
chain, the suppression of the reproductive functions of organisms, the
additive and synergic effects of toxic factors, the varying resistance
of organisms of various systematic groups, etc.

In conclusion, let us emphasize once more the very important, in
our opinion, large-scale situation of superimposition of the band of
maximum pollution on the band of maximum biologic productivity of the
world ocean--the neritic zone of the temperate latitudes of the northern
hemisphere. It is in this very area, with its constantly increasing
background level of man-made impurities, that the effects and anomalies
which we have been discussing arise and propagate throughout the entire
ocean. It is here that both national and international efforts should
be concentrated for the protection of the marine environment from
pollution.

417

2 . Accumulation of Radionuclides by Hydroblonts and Its Results.
(G. 6. Polikarpov)

The accumulation of radionuclides, like other substances, by marine
organisms is one difference between the processes by which they reach
the environment and are removed from the environment. In the extreme
case, when removal can be ignored, for example in the building of
skeletons, the maximum capability of hydrobionts for accumulation of an
element and its radioactive isotopes from the marine environment is
revealed, that is, practically all of the element is accumulated. For
example, the skeleton of Acantharia consists of strontium sulfate;
therefore, their spicules contain 6 10^ times more strontium (and Sr^^)
than the environment. The shells of mollusks are constructed of calcium
carbonate in the process of biologic extraction of calcium from sea
water. In addition to the practically permanent store of Sr in the
spicules of the Acantharia or Ca in the shells of the mollusks, these
and other elements are metabolized in their bodies. The higher the rate
of excretion, the lower (in the case of the excreting store of the
element and its radioisotope) the level of accumulation of the substance
in question. When the rates of excretion are similar to the rates of
accumulation of an element (radionuclide) is prevented and the result is
identical to the result of processes which prevent penetration of the
element (radionuclide) through the tissue and membrane barriers.

Of course, during a period of time which is short in comparison to
the life cycle of the organism the accumulation is not great, since it
involves only the quantity of the corresponding element (radionuclide)
and population of its carrier which are present. The maximum possible
accumulation in all of the stores, including those which have little or
no exchange with the environment, occurs when an element (or
radionuclide) is constantly present in the environment throughout the
entire life cycle of an organism. If the organism is exposed only to
rapidly exchanging supplies of a given element (radionuclide),
relatively brief contact of the organism with the element (radionuclide)
may be sufficient. This is also correct if the element (radionuclide)
is accumulated only by adsorption from solution (in the form of ions,
suspensions, on micelles, etc.). Therefore, the accumulation factors
must be subdivided into saturated and unsaturated factors.

Values of concentration function. --The many reports which have been
published on the accumulation coefficients of the chemical elements
whose radionuclides are formed upon nuclear explosions or operation of
nuclear enterprises are summarized in Table 4. The range of these
coefficients is great: from insignificant (1) to tremendous (10 ). For
many elements, a similarity is observed between the values of
accumulation coefficients for all trophic levels, while for some a
decrease or, conversely, an increase is observed at the level of the
predators.

418

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419

The values of the concentration function of plankton in
relationship to a number of elements are quite great. For example 1 g
of plankton ash concentrates in itself a quantity of boron equal to its
content in 32 ml of sea water, along with a quantity of aluminum equal
to its content in 300 1 of sea water.

Plankton also quite actively concentrates P, Cu, Cd, Ti, Cr and
other elements. Significant concentration of radionuclides by pelagic
crustaceans occurs during the first hours after the beginning of
exposure. For example, the Copepoda, during the first three hours,
usually accumulate from one third to one half of the quantity of Mn and
Co°^ which they accumulate over the next two days. Our attention is
drawn by the nonuniformity of accumulation of radionuclides by different
individuals of the same species. Usually, the young members of the
species concentrate these elements more rapidly than mature members.
This phenomenon has been specially studied from the standpoint of its
significance for the formation of absorbed doses of ionizing radiation
from the radionuclides accumulated by hydrobionts (Ivanov, Parchevskaya,
1975).

Radioactivity of the environment and its significance in the life
of hydrobionts. --A comparison of the absorbed doses of various
radionuclides in the tissues of a number of animals of the Sea of
Okhotsk and the Bering Sea (herring, seal, whales) shows that the
primary contribution is made by K^^, with artificial radionuclides
(Cs^-^ , Sr^^, Y^^) playing a secondary role.

A comparison of the doses accumulated in the Sea of Ireland by
phytoplankton and zooplankton, mollusks and crustaceans, benthic and
pelagic fish, from the natural background, global radioactive fallout
and the dumping of radioactive wastes in the vicinity of Windscale has
shown that the global fallout usually does not exceed the contribution
of the natural background radiation. However, the wastes dumped into
the Irish Sea by the Windscale enterprises create a dose level which is
higher than the natural background: for phytoplankton by a factor of
something over 10, for zooplankton by a factor of over 100, for the
benthos and fish--by a factor of up to 100.

Various organisms differ sharply in their sensitivity to ionizing
radiation. „Most sensitive are certain crustaceans and fish. Beginning
with an SR^^-Y^^ concentration of 10'^ curies/1 or higher, the frequency
of nuclear disorders in a number of marine fish increases (Tsytsugina et
al., 1973). The sensitivity of the larvae of two species of sea
urchi ns--Pseudocentrotus depresus Anthoci dari s crass i spi na--to the
concentration of tritium differs by a factor of 10"^ (Akita, Shiroya,
1970).

Due to experimental difficulties, there has been insufficient
material gathered to draw general conclusions in the area of the effects
of radioactive pollutants on the populations and ecosystems in the seas
and oceans. This is a matter which should be taken up in the near
future, considering the rapid rates of growth of nuclear power
engineering.

420

3. Anthropogenic Thermal Effects on the Population of the Sea.
(S. A. Mileikovsky)*

One component of anthropogenic pollution of marine coastal and
estuarine waters is so-called "thermal pollution," the dumping of heated
water into the sea, after it has passed through the water-cooling
systems of electric power plants and industrial enterprises. Evaluating
the influence of various components of anthropogenic pollution of sea
water on its living resources, Dybern (1974) included thermal pollution
in the second most harmful category of "significant pollution factors"
of the sea.

Special studies and calculations have shown that as the power of an
electric power plant or industrial enterprise increases, the available
reserves of fresh water become insufficient to support normal operation
of the water-cooling system. Due to this, an increasing number of these
enterprises will be placed on the shores of estuaries and bays,
utilizing the more abundant supplies of water which they provide. For
example, it was calculated for the USA (Picton, 1960) that by 1980, 32%
of all thermal electric power plants in the nation would be located near
estuaries. This tendency toward placement of electric power plants and
industrial enterprises along the sea coast means that the volume of
thermal pollution of marine coastal and estuarine waters will increase
and its significance as an ecologic factor will grow.

3.1 Amount of Thermal Pollution of Marine Coastal and Estuarine
Waters, Temperature of Waters Dumped and Changes in"
Temperature of Natural Waters which Result

The total amount of thermal pollution of the sea has never been
calculated, although some idea of the scale of the phenomenon can be
gained on the basis of a number of data. Along the east coast of the
USA by late 1968 there were 86 electric power plants burning fossil fuel
(coal, oil), dumping their heated water into estuaries, bays and fresh
water bodies near the sea (Sorge, 1969). On the west coast of the USA,
electric power plants with a total power capacity of 17.2 million kW
were dumping their heated waters into the sea, and in California the
capacity of these power plants represented 85% of the total electric
power generating capacity in the state (North, Adams, 1969). It has
been calculated (Mihursky et al . , 1970) that in the USA some 4 million
m'^ of fresh and sea water are utilized for water cooling of electric
power plants and industrial enterprises e\/ery minute of every day; the
temperature of the water dumped is 5 to 15°C higher than the temperature
of the natural waters receiving the heated water.

*Deceased.

421

In Japan, nuclear electric power plants alone will consume 130,000
m-^ of sea water permitted for cooling purposes by 1980 (Niva, 1973).

The Hunterstone nuclear power plant (in Scotland) dumps 91,000 m-^
of water with a temperature of water 8-10°C higher than the natural
water into the Firth of Clyde each hour. As a result, the surface
temperature in the region of this thermal pollution is increased by 3-
5°C (Barnett, 1971, 1972).

Usually, the temperature of water dumped by electric power plants
and industrial enterprises is 5 to 13°C higher than the temperature of
the natural waters, and in some cases it has been heated by as much as
14-24°C.

Regular thermal pollution changes the annual course of temperature
of natural waters. For example, at Marchwood on the south coast of
England, before construction of the thermal electric power plant in the
mid-1950' s, the minimum temperature of the surface water (February) was
1-2°C (in 1954, the temperature dropped to -1°C) while the maximum (in
August) was 22°C; after the power plant went on stream, the temperature
never dropped below 6.5°C in winter and in summer it rose to 26.5-27°C
(Raymont, Carrie, 1964).

In Copenhagen Harbor, the water temperature near the area of
thermal pollution of one factory reached 6°C even in winter, while in
Southhampton Harbor, 400 m from the thermal dump of an electric power
plant, it was 3°C higher than the natural temperature, and in the
discharge canals of electric power plants in the Patuxent River estuary
(Chesapeake Bay) it was 6.3°C higher, and in Biscayne Bay (Florida)--5''C
higher than the temperature of the natural water receiving the thermal
discharge (Naylor, 1965b; Nauman, Cory, 1969; Thornhaug et al . , 1973).

3.2 Influence of Thermal Pollution on the Conditions of Existence
of Flora and Fauna

The dumping of heated waters into the sea leads to an increase in
the temperature of the natural waters of the region, a decrease in their
oxygen content, a decrease in viscosity, a shift of the hydrologic
seasons in the surface layers (abnormal lengthening of the hydrologic
summer). These changes, in turn, lead to changes in the nature of
circulation of water in bays and estuaries, stagnation of water, and
increase in the rate of sediment formation and silting, particularly in
the sunrmer.

The effect of thermal pollution on the aquatic communities of the
estuaries, bays and other marine coastal areas can be quite varied in
form, being direct and indirect, ranging from very strong to weak.
Heating of natural waters by 4-6°C (and in the summer, sometimes, by
only l°C--Bush et al . , 1974) may result in the death of a number of
stenothermal species, suppression of the breeding of many species,
changes in the specific composition of communities due to replacement of
local species with thermophilic intruders, changes in many biologic
characteristics of local species--metabolism, shape formation of
colonial animals, behavior, nutrition, etc. This heating may lead to a

422

decrease in the intensity of photosynthesis of plants, an increase in
oxygen consumption in animals due to intensification of metabolism
(which, when the oxygen content of the water is reduced, has a harmful
influence on them), an increase in the susceptibility of local species
of animals and plants to various toxic substances and pathogenes,
possibly causing massive death of species. As a result of the
stagnation of water caused by thermal pollution, there may be cases of
massive development of algae and, consequently, processes of decay,
which have a depressing effect on many species. Thus, thermal pollution
disrupts the normal ecologic balance of communities inhabiting the
natural waters in the area of the thermal discharge.

For example, in Chesapeake Bay, under the influence of thermal
pollution, a population of commercially valuable soft-shell clam. My a
arenaria, died and was replaced by the small, noncommercial species
Gemma gemma, which has a higher level of heat tolerance (Kennedy,
Milhursky, 1971). In the region of Cape Cod, thermal pollution, on the
other hand, stabilized the population of the mussel Hytilus edulis, by
depressing the feeding of its primary enemies--the sea star Asterias
forbesi , the dog-whelk Thais lapillus and the crab Carcinus maenas
(Pearce, 1969).

The decrease in the population of the bivalve Mulinia lateralis in

the waters of the Atlantic coast of the USA, resulting from thermal

pollution, has significantly harmed water birds, for which it was a diet
staple (Kennedy et al . , 1974).

3.3 Influence of Thermal Pollution on the Distribution of Flora
and Fauna"

Benthos. --Examples of the influence of thermal pollution on the
benthos have been accumulated for some time, primarily for various areas
along the Atlantic coast of the USA. In the estuary of the Patuxent
River and a number of other areas of the Chesapeake Bay, thermal
discharges have greatly decreased the areas of the plant Ruppia
maritima, while increasing the biomass, population and density of
epifauna' (Anderson, 1969; Cory, Nauman, 1969; Nauman, Cory, 1969). In
Biscayne Bay, thermal pollution caused disease, then death of blooming
plants and macrophytes and changes in the composition of the zoobenthos
(Roessler, zieman, 1969; Wood, Zieman, 1969; Thornhaug et al . , 1973).
In other areas of the Florida coast, thermal pollution has been found to
influence the distribution and migration of the commercial blue crab
Callinectes sapidus (Nugent, 1970; Leffler, 1972).

In one bay along the California coast, in a heated area, the
species variety of bivalve mollusks increased, while in other bays the
composition of benthic communities changed (North, 1968).

Thermal pollution in Hawaii caused the death of corals in the
region of the thermal discharge and the transformation of the reef to
dead limestone covered with sand (Jokiel, Coles, 1974). Changes in the
benthos of the Baltic Sea coastal area, observed by Swedish
investigators in an area of thermal discharge from a 3 million kW
nuclear power plant were similar to those observed in natural waters

423

during the hot summer of 1968, when the water temperature was 9-10°C

higher than usual for a period of 3 weeks (Ankar, Jansson, 1973). There

are other examples of the influence of thermal pollution on the
distribution of the benthos.

Plankton. --Data on the influence of thermal pollution on the
distribution and composition of plankton are as yet sparse. For
example, it has been shown that in the vicinity of Southhampton (Pannel
et al., 1962; Raymont, 1964; Raymont, Carrie, 1964), thermal pollution
has caused a gradual increase in the population of the warm-water
copepod Acartia tonsa, and in the summer plankton the larvae of the
warm-water cirripedian El mini us modestus have become numerically
dominant, quite unusual for northern European waters. On the other
hand, in the Patuxent River estuary, the thermal discharge did not cause
changes in seasonal parameters of the distribution of Acartia tonsa and
Eurytemoraaf finis (Heinle, 1969b). Similarly, off the coast of Japan,
the thermal discharge of nuclear power plants in most cases did not
result in a decrease in the population of zooplankton, and in many cases
there was even an increase in its population (Niva, 1973).

Fish. — Depending on the thermopathy, various species of fish are
attracted to or repelled by regions of thermal discharge. In western
European waters, for example, cases of winter concentration of a number
of fish in regions of thermal discharge have been observed.

3 . 4 Passage of Pelagic Fish through the Pipes of Water Cooling
Systems of Nuclear Power plants and Industrial Enterprises

One very important form of thermal pollution is its effect on
pelagic animals as they pass through the pipes of the cooling systems of
power plants and industrial enterprises. Passage through the pipes has
different effects on different organisms, and this phenomenon itself may
lead to different ecologic results. In the Patuxent River estuary,
passage of phytoplankton through the pipes of the cooling system of the
power plant in the summer inhibits photosynthesis, while in the winter
it cancels the stimulating effect of the increased temperature of the
water on photosynthesis; as a result, it may lead to a decrease in the
photosynthetic activity of the phytoplankton by a factor of 10 (Morgan,
1969). Inhibition or stimulation of the photosynthesis of phytoplankton
as it passes through the cooling pipes of electric power plants have
also been observed in the York River estuary in Virginia (Warinner,
Brehmer, 1966).

Many planktonic copepods die, primarily as a result of mechanical
damage, as they pass through the cooling system of the power plant in
the Patuxent River estuary, and 90% of zooplankton eggs lose their
capacity to hatch (Heinle, 1969a); in the water cooling pipes of a power
plant near New York, from 70 to almost 100% of the copepods died
(Suchanek, Grossman, 1971; Carpenter et al . , 1974).

It has been shown for Acartia tonsa (Reeve, Cosper, 1970) that if
it is held at temperatures characteristic of the thermal discharge
waters dumped into Biscayne Bay, the mortality rate is twice as high in
winter as in sunmer. However, the larvae of bivalve mollusks can pass

424

through the water cooling pipes of power plants without harm and settle,
forming normal populations in thermal discharge regions (Adams, 1969;
Barnett, 1972).

It has been thought that the juveniles of various fish can pass
through the water cooling pipes of power plants without harm (Kerr,
1953; Markowski, 1959). New studies (Marcy, 1971), however, have shown
that the mortality of fry is very high in such situations.

Thus, water cooling systems of power plants and industrial
enterprises located along sea coasts and estuaries have a significant
influence on the population and reproduction of plankton, benthos and
nekton.

3.5 Change in the Specific Composition on Communities in Regions
of Thermal Discharge

The change in the specific composition in regions of thermal
discharge has been most thoroughly studied for coastal benthic
communities. The barnacle Balanus amphi trite, entering western European
waters from the subtropics and tropics, has formed stable populations in
regions of thermal discharge along the coasts of southern England, Wales
and Holland (Stubbings, Houghton, 1964; Nlaylor, 1965a; Borghouts-
Biersteker, 1969). Near Southhampton, in the area of thermal discharge
from the Marchwood electric power plant, a stable, self-reproducing
population of the bivalve mollusk Mercenaria mercenaria has formed--an
intruder from the northwest Atlantic (Ansell, 1969). Tn Swansea Harbor
(Wales), due to the heating of the water by the thermal discharge of a
power plant, new warm-water species of corals, polychaetes, bryozoans,
camptozoans, cirripedians, isopods and fish have appeared, some from
subtropical and tropical waters, some from the warm- temperate regions
located to the south; at the same time, a number of local species have
disappeared from the benthos at the point where the warm waters are
discharged (Naylor, 1965a).

A similar picture has been observed for the coastal benthos and
nekton in many other regions damaged by thermal pollution.

3.6 Influence of Thermal Discharge of the Biology of Organisms

The influence of heating of waters on the biology of organisms may
be either negative or positive. Thermal pollution may influence the
intensity of photosynthesis of phy topi ank ton, accelerate the occurrence
of biochemical processes in organisms and increase their susceptibility
to disease. Heating of water influences the intensity of respiration,
the stability and integrity of leaves and stolons of littoral and
sublittoral blooming plants and macrophytes. In the estuaries of
Florida, the turtle grass Thalassia testudinum has lost some of its
leaves under the influence of thermal discharge, but retained healthy
stolons; however, in cases of severe and permanent heating, the
accumulation of heat by sediment has resulted in loss of strength by the
stolons, which are then broken (Wood, Zieman, 1969).

425

Thermal pollution changes the seasonality and intensity of
migration of a number of benthic invertebrates, the feeding rate (which
sometimes decreases, sometimes increases), the growth rate (which
increases), the maximum size and size upon achievement of sexual
maturity, shell thickness, volume of accumulation of various chemical
elements in the body tissues (for example, oysters accumulate an excess
of copper, which has a depressing effect on them).

Thermal pollution has a severe effect on breeding, larval
development and reproduction of organisms in the sea and estuaries,
particularly benthic invertebrates in the vicinity of the thermal
discharge (Davis, 1972; Verwey, 1973; Mileikovsky, 1976). The most
usual result of this effect is earlier beginning and longer duration of
the periods of breeding and spawning. This picture was observed for
benthic invertebrates in regions of thermal discharge of electric power
plants along the coasts of England, Wales, Scotland and the USA (Pannell
et al., 1962, Naylor, 1965a, b; Adams, 1969; Barnett, Hardy, 1969;
Barnett, 1971, 1972). Induction of reproduction out of season has also
been noted for marine plants (Wood, Zieman, 1969). The earlier
beginning and longer duration of the reproductive and spawning season
usually give the species involved certain advantages and increase their
competitiveness, although at times the earlier beginning of spawning
simply means that some of the fry die because they are hatched too early
(Barnett, Hardy, 1969).

In temperate and cold waters, thermal pollution creates favorable
conditions for the reproduction of various intruders from warmer waters
(Ansel! , 1963; Raymont, Carrie, 1964; Stubbings, Houghton, 1964; Naylor,
1965a, b; Adams, 1969).

Under the influence of the heating caused by thermal discharge, the
duration and time of settlement of pelagic larvae of some forms of
benthic invertebrates change (becoming longer for most species), the
nature of succession changes, and the settling rate increases. All of
this results in the formation of more abundant epi fauna in regions of
thermal discharges, and sometimes of infauna as well, than in normal
areas.

3.7 Degree of Harm of Thermal Pollution of Marine Coastal and
Estuarine Waters"

The question arises: what is the specific harm of thermal
pollution at its present level of intensity? The data which have been
gathered indicate that in most cases, the harmful effect is not very
strong, and is manifested in small regions in the immediate vicinity of
the discharge of heated water. Based on the fact that the effect of the
thermal discharge of the Hunterstone nuclear power plant (Scotland) on
the fauna of the Firth of Clyde is quite limited, it has been assumed
that in the temperate latitudes, thermal pollution, at today's scale,
will have no harmful influence on the marine biota. However, should the
volume of thermal pollution increase in the future, unexpected ecologic
effects may occur (Barnett, 1971).

426

Since the volume of thermal discharge into marine coastal and
estuarine waters continually increases, the question of the development
of methods of checking the effects of thermal pollution takes on
particular significance. The protective measures which have been
suggested are few and sometimes contradictory. All authors agree that
the most important thing is to provide the most rapid possible mixing of
the heated discharge water and natural water, to cool the warmer water
to the natural level as quickly as possible. To do this, it has been
suggested that electric power plants and manufacturing plants either be
constructed along open areas of the sea coast with surf, and the thermal
water be discharged at some depth (Glooschenko, Glooschenko, 1969), or
that heated water be discharged into special mixers (Verwey, 1974) or
into the open sea (Barnett, 1972). However, it has been noted that
estuarine biota have been adapted by evolution to great fluctuations in
environmental factors, including temperature, much better than the biota
of open sea coasts (Cairns, 1969; Brungs, 1970; Patric, 1972).

We must not forget the possibility of using thermal discharge to
meet the economic needs of man. Heated water can be used to develop the
farming of commercial species of algae, invertebrates and fish in
regions of thermal discharge. The first experiments along this line
have already been undertaken in several countries. The possibility has
also been reported of increasing the effectiveness of reproduction of
fish and invertebrates in cold-water regions by the use of heated water
(Davis, 1972), as well as the use of heated water to control fouling
(Naylor, 1965b).

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