Advances in Marine Biology, Volume 9

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Advances in

MARINE BIOLOGY VOLUME 9

This Page Intentionally Left Blank

Advances in

MARINE BIOLOGY VOLUME 9 Edited by

SIR FREDERICK S. RUSSELL Plymouth, England

and

SIR MAURICE YONGE Edinburgh, Scotland

Academic Press London and New York

1971

ACADEMIC PRESS INC. (LONDON) LTD. BERKELEY SQUARE HOUSE BERKELEY SQUARE LONDON, W l X 6BA

U.S. Edition published by ACADEMIC PRESS INC.

111 FIFTH AVENUE NEW YORK, NEW YORK 10003

Copyright

0 1971 by Academic Press Inc. (London)Ltd.,

All rights reserved

N O PART OF THIS BOOK MAY BE REPRODUCED IN ANY FORM BY PHOTOSTAT,

MICROFILM, OR ANY OTHER MEANS, WITHOUT WRITTEN PERMISSION FROM THE PUBLISHERS

Library of Congress Catalog Card Number: 63-14040 ISBN: 0-1 2-026109-X

PRINTED IN QREAT BRITAIN B Y THE WHITEFRIARS PRESS LTD. LONDON AND TONBRIDQE

CONTRIBUTORS TO VOLUME 9 J. A. ALLEN, Dove Marine Laboratory, University of Newcastle upon Tyne, Cullerwats, North Shields, Northumberland, England.

N. BALAKRISHNAN N u , The Marine Biological Laboratory, University of Kerala, Trivandrum-7, Kerala, India.

E. D. S. CORNER,Marine Biological Association of the United Kingdom, The Laboratory, Citadel Hill, Plymouth, Devon, England.

D. H. CUSHING), Fisheries Laboratory, Lowestoft, Suffolk, England. ANTHONYG. DAVIES,Marine Biological Association of the United Kingdom, The Laboratory, Citadel Hill, Plymouth, Devon, England.

M. R. GARRETT,Dove Marine Laboratory, University of Newcastle upon, Tyne, Cullercoats, North Shields, Northumberland, England. R. H. MILLAR,Scottish Marine Biological Association, Dunstaffnage Marine Research Laboratory, Oban, Argyll, Scotland. M. SARASWAT~EY, Indian Ocean Biological Centre, N a t i o d Institute of Oceanogrqhy, Cochin, India.


CONTENTS CONTRIBUTORSTO VOLUME 9

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The Biology of Ascidians

R.H. MILLm I. Introduction

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11. Feeding A. The Feeding Mechanism B. Food.. .. ..

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HI. Breeding

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A. Breeding Season B. Spawning .. C. The Larva . .

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IV. Life Cycle: Growth, Succession of Generations and .. Mortality .. .. .. .. 0

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.. V. Ecology . .. A. The Numbers and Biomass of Ascidians . .

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B. Changes in Populations .. C. Factors Affecting Distribution and Abundance. .

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VI. Predators, Parasites, Commensals and Symbionts

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A. Predators .. .. B. Commensals, Parasites and Symbionts

VII. Geographical Distribution A. Shallow-WaterAscidians B. Deep-Water Ascidians vn

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65 66 69

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CONTENTS

VIII. Economic Importance . . .. .. A. Fouling .. .. .. .. B. Food of Man, and of Commercial Fish C. Uptake of Harmful Substances . . IX. References

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Plankton as a Factor in the Nitrogen and Phosphorus Cycles in the Sea

E. D. S. CORNERAND ANTHONY G. DAVIES I. Introduction

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11. The Chemical Forms of Nitrogen and Phosphorus Dissolved in Sea Water . . .. .. * . 102 A. Inorganic Nitrogen.. *. .. .. 103 B. Physico-chemical Reactions .. .. 104 C. Organic Nitrogen . . .. .. .. 104 D. Inorganic Phosphorus .. .. .. 105 E. Organic Phosphorus .. .. .. * . 105

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111. The Stoichiometry of Biologically Induced Changes in Nutrient Levels . . .. .. .. * . 106 A. The " Assimilation Ratio ", d N : d P . .. 106 B. Apparent Oxygen Utilization . .. .. 109 # .

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IV. Uptake of Nitrogen Compounds by Phytoplankton A. Inorganic Forms of Nitrogen .. B. The Effect of Light. .. .. .. C. The Hyperbolic Relationship . . ..

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113 113 116 117

V. Uptake of Phosphorus Compounds by Phytoplankton. . 121 A. Inorganic Forms of Phosphorus .. .. .. 121 B. Organic Forms of Phosphorus .. 121

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OONTYINTS

VI. The Effect of Nutrient Levels on Phytoplankton

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Growth Kinetics

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VII. Nitrogen and Phosphorus Levels in Phytoplankton . . 126 A. Release of Organic Forms of Nitrogen and Phosphorus by Phytoplankton . .

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VIII. The Assimilation of Nitrogen and Phosphorus by Zooplankton . . . * .. .. A. Living Diets. .. B. Detritus . . .. .. C. Dissolved Organic Material .. D. Laboratory Studies on Assimilation E. Superfluous Feeding .. ..

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.. Nitrogen and Phosphorus Excretion by Zooplankton. . A. Nitrogen Excretion. . .. .. .. .. B. Phosphorus Excretion . . .. .. ..

IX. Levels of Nitrogen and Phosphorus in Zooplankton X.

128 129 130 130 132

136 140 145 145 152

C. Seasonal Surveys of Nitrogen and Phosphorus Excretion . . .. .. .. .. .. 156 D. Nutrient Regeneration .. 160

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XI. Growth of Zooplankton in Terms of Nitrogen and Phosphorus .. .. .. .. ,. 162 A. Rate of Growth . .. .. .. .. 162 B. Egg Production .. .. 166 C. Net and Gross Growth Effioiencies .. .. 165

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XII. Plankton Production and Nutrient Levels in Certain Sea Areas .. .. .. .. .. A. Temperate Regions. . .. .. .. .. B. Tropical and Sub-tropical Regions . . .. C. Polar Regions . . .. .. .. .. D. Partially Enclosed Sea Areas . . .. ,.

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CIONTENTS

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XIII. Acknowledgements

XIV. References

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Taurine in Marine Invertebrates

J. A. ALLENAND M. R. GARRETT

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I. Introduction

II. Chemistry 111. Function

IV. Summary and Conclusions V. Acknowledgements VI. References

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Upwelling and the Production of Fish D. H. CUSHMU

I. Introduction

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11. "he Physical Background

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256

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111. The Biological Background . . .. .. .. 264 A. The Production Cycle in an Upwelling Area . . 264 B. The Part played by Nutrients in an Upwelling . .. 267 System

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IV. Description of a Well-known Upwelling Area A. The California Current System B. The System in the Gulf of Panama

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a0NTENTs

V. The Upwelling Areas

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A. The Width of the Upwelling Zone .. .. B. Upwelling Areas in the Eastern Boundary Currents . .. .. .. .. C. TheIndianOcean .. .. .. D. The Equatorial System .. .. E. Domes and the Eastern Boundary Currents . . F. Minor Upwellings . . .. .

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284 288 291 292 293

VI. The Production of Living Material in the Upwelling .. Areas .. A. Primary Production *. .. B. The Production of Zooplankton C. The Production at the Third Trophic Level .. D. The Transfer Coefficients . ..

294 294 301 306 310

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.. The Systematics and Distribution of the Teredinidae . .

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.. References . .

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VII. The Biology of an Upwelling Area

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The Biology of Wood-boring Teredinid Molluscs N. BALAKRISHNAN NAIRAND M.SLBASWATHY

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I. Introduction 11.

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111. Morphological and Anatomical Studies..

IV. The Sexual Phases V. Fecundity

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OONTENTS

VII. Breeding Sectson VIII. Fertilization

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IX. Embryology and Larval Development A. The Gametes .. .. B. Development .. .. C. Duration of the Larval Period .. D. Food of the Larvae.. E. Settlement . . ..

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X. The Season of Settlement

XIII. Growth Rates

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XIV. Dispersal of Shipworms

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Physiological Studies

XVI. Food and Digestion

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XI. The Pattern of Vertical Settlement XII. Teredinids in Deep Water

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447 452 456 457 467 457 458 469

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I. Oxygen Content of the Water J. Hydrogen-ion Concentration K. The Effects of Turbidity . . L. The Effects of Pollution . M. The Effect of Marine Foulings N. Relation to other Borers . . 0. Parasites and Associates . .

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XVIII. Objects Attacked

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XIX. Detection and Prevention of Shipworm Attack XX. Timbers of Unusual Durability against Shipworms A. The Role of Silica . . .. B. Bark of Trees

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AUTHOR INDEX ..

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TAXONOMIC INDEX

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SUBJECT INDEX ..

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XXI. Acknowledgements XXII.

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References

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CUMULATIVEINDEX OF AUTHORS CUMULATIVE INDEX OF TITLES

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Adv. mar. Biol., Vol. 9, 1971, pp. 1-100

THE BIOLOGY OF ASClDlANS R. H. MILLAR Dunstaffnuge Marine Research Laboratory, Oban, Argyll, Scotland.

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I. Introduction . .. 11. Feeding .. .. .. A. " h e Feeding Mechanism .. . . . . B. Food . . . . .. .. .. .. .. 111. Breeding .. A. Breedingseason . . . . . . . . . . B. Spawning C. TheLenre IV. Life Cycle: Growth, Succession of Generations and Mortality . . . . . . . . . . . . V. Ecology . . . . A. The Numbers and Biomass of Ascidians . B. Changes in Populations .. .. .. C. Factors Affecting Distribution and Abundance VI. Predators, Parasites. Commensals and Symbionts . A. Predators . . . . . .. .. .. B. Commensals, Parasites and Symbionts . . . . .. . . . . VII. Geographical Distribution A. Shallow-water Ascidians .. .. B. Deep-water Ascidians . . . . .. .. Economic importance . . . . . . .. .. VIII. A. Fouling . . . . .. . . . . B. Food of Man, and of Commercial Fish .. C. Uptake of Harmful Substances .. . . . . . . Ix. References

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I. INTRODUCTION Ascidians have been studied from many viewpoints, and a simple analysis of the entries in the Zoological Record indicates the main interests of recent investigators. Amongst publications appearing, for instance, between 1963 and 1967 and dealing in part or whole with the group, the number of papers having at least some mention of the various subjects used in classifying the entries is as follows : general literature, 70 ; structure, 117 ; physiology, 151 ; reproduction, 34 ; development, 168; evolution and genetics, 31 ; ecology and habits, 90; distribution, 77. Since structure is taken to include histochemistry and cytochemistry, and development to include chemical embryology, it is 1

2

R. H. MILLdR

evident that physiological, chemical and biochemical studies accoiint for a large proportion of the recent research on ascidians. These aspects are not treated in the present review, which aims rather to survey advances in our knowledge ofthe animal as a whole living organism. Much of the work on structure, evolution and genetics, and most physiological studies are therefore also excluded. No way of selecting topics is entirely satisfactory and the inclusion of some papers and the omission of others may seem arbitrary. Another difficulty in preparing a review of this nature is to decide how old a publication may be and yet be regarded as an advance. I have not chosen a date, but have been guided by whether the matter in a paper has already been dealt with in a review or major contribution devoted to ascidians.

11. FEEDING

A. The feeding mechanism It has long been known that ascidians feed by filtering organisms and particles from water drawn into the branchial sac through the oral siphon and expelled through the atrial siphon, and that the process involves mucus secreted by the endostyle. Early accounts differ somewhat in detail; thus Roule (1884) described the mucus as passing out from the endostyle and across the inner faces of the branchial walls, where food particles are trapped, but Herdman (1899) thought that food was retained by mucus a t the entrance to the branchial sac. Orton (1913) and Hecht (1918) confirmed Roule’s account of the process. In some particulars, however, Hecht’s description has been modified by subsequent work. He believed that food particles are retained by the stigmata (the openings in the branchial wall) and are trapped in mucus only after being passed by cilia t o the tips of the branchial papillae. But MacGinitie (1939) found that continuous mucous sheets on the branchial walls trap particles from the water before it passes out through the stigmata. This was confirmed by Jmgensen (1949), Jmgensen and Goldberg (1953), Millar (1953a), and Werner and Werner (1954). Although most observers seem to have assumed that ciliary action alone is responsible for moving the mucous sheet towards the roof of the branchial sac, it is possible that muscles play some part, and Hecht (1918) described waves of contraction which bring adjacent rows of papillae together so that the sheet is pushed or pulled across the branchial wall. It is, however, by no means certain that such a process is part of the normal pattern of feeding, neither Werner and Werner (1954) nor Millar (1953a) having observed it in Ciona intestinalis (L.). When it reaches the roof of the sac, the endless filter of mucus is

TEE BIOLOOY OF ASCLDIANS

3

gathered by the dorsal lamina or languets and rolled into the form of a cord, which is then pulled into the oesophagus (Millar, 1953a). Jergensen (1949) investigated the efficiency of particle retention in Molgula sp. and Ciona intestinalis, and found that particles of colloidal graphite of 2-46 p were retained by the mucous sheet. In later experiments J~rgensenand Goldberg (1953) showed that Ciona can completely remove graphite particles of 1-2 p, but that protein molecules (haemocyanin and haemoglobin) mainly escape. The fact that some protein molecules are captured, however, suggests that processes other than purely mechanical ones may be involved. Korringa (1952) believed that the electrical charges on the mucus and the food particles of filter-feeding animals may determine whether or not small particles, and molecules, are trapped. I n this connection it is worth noting that vanadium, which is present in high concentrations in certain ascidians, appears to be taken up from the sea water initially by adsorption on the mucus of the branchial sac (Goldberg et al., 1951 ; Bielig et al., 1961). Stephens and Schinske (1961) found that the three species of ascidians which they investigated all removed considerable quantities of amino acids from solution, but there was no direct evidence that mucus was responsible. Not all organisms in the feeding current reach the mucous sheets, since the oral tentacles retain many of the larger particles (Werner and Werner, 1954) and those which reach the branchial sac may fail, in some unknown way, to be incorporated in the mucous sheets, and ase subsequently expelled through the oral siphon (MacGinitie, 1939). Moreover, MacGinitie briefly mentioned the rejection of some particles already caught by mucus and suggested that " cilia bordering the dorsal groove " may be responsible. This interesting possibility deserves further study, since rejection mechanisms play an important part in filter-feedingmolluscs, and might be expected to occur also in ascidians. Although we have little indication of how rejection might take place, there is some indirect evidence that it does, for in Dislaplia cylindricu (Lesson) and Eugyra aernbaeckae Millar the branchial sac was found to contain a mixture of sand and cells of ph-ytoplankton, but in the stomach only the cells were present (Millar, 1960). The basis of selection is apparently not merely the size of particle, since the stomach contained cells as large as the sand grains which had been rejected. Ascidians can also control their feeding by cutting off the secretion of mucus from the endostyle, with or without maintenance of the water current (MacGinitie, 1939 ; Werner and Werner, 1954). The efficiency of feeding depends not only on the ability to filter a wide range of particles but also on the rate of water transport. This has

4

a. E. M&LAR

been measured using various experimental methods, by Hecht (1916), Jrargensen (1949, 1952), Goldberg et al. (1951), Hoyle (1953) and Cnrlisle (1966). The results vary considerably. Thus Hecht estimated 80 ml/h per g wet weight of animal in the case of Ascidia atra Lesueur, and Jrargensen’s value for Molgula was 540ml/h per g wet weight. It is probable that performance under favourable natural conditions will be higher than in experiments, particularly in those involving considerable interference with the animal, such as Hecht’s method using a tube inserted into the siphon. Hoyle’s (1953) criticism of Hecht’s work is partly invalid, since he failed t o realize that Hecht measured particle velocity in the inhalent, not the exhalent, current. Hoyle believed that ciliary currents would provide insufficient food and oxygen. He measured the water exchange resulting from spontaneous rhythmic contractions in Phallusia mammillata (Cuvier)and concluded that these introduced much more water than the ciliary current. The process he visualized consists of water being drawn into the branchial sac during relaxation of the body, and the water being filtered on the branchial walls with the aid of ciliary currents. However, Jnrrgensen (1955) did not accept this idea and calculated that in Ciona at least 30 times as much water is transported by ciliary action as by rhythmic contractions. One advantage claimed for feeding by body contractions is the ability to regulate the rate of feeding by varying the frequency of contraction, and Hoyle found the frequency to increase at lower food concentrations. It is evident that the role of spontaneous contraction needs further investigation, especially in relation to feeding. Indirect evidence for the adequacy of ciliary currents is based on the available particulate organic matter in the sea, and Jnrrgensen (1955) concluded that ascidians can meet their needs from this source.

3. Food Despite our knowledge of the mechanism of feeding, little is known of the food itself. Phytoplankton and organic particles in suspension apparently constitute the bulk of the food of many species. For instance, in Paramolgula gregaria (Lesson),a mainly Subantarctic species which attains a length of over 20cm, the gut was found to contain principally unicellular planktonic algae and diatoms, and only a little sand and animal remains (Millar, 1960). The waters of the Patagonian Shelf, where the specimens were collected, are rich in phytoplankton which, not surprisingly, constitutes the food of even such a large-bodied species. And in Microcosmus sulcatus (Coquebert) the branchial sac has been found to contain organisms (bacteria, diatoms and radiolarians) characteristic of the water immediahly above the substratum (Costa,

TEE BIOLOGY OF ASCIDIANS

6

1960). In other species the gut contents vary, perhaps according to the local water conditions. Kott (1952, 1964) and Millar (1955a, 1963, 1966a) noted large quantities of mud in the gut of Ascidia sydneiensis Stimpson, but the same species may contain algal cells, diatoms and peridineans, with little inorganic matter (Millar, 1960). Subtle differences appear to exist in the food of related species living in the same area, as with Ascidia nigra (Savigny) and A . interrupta Heller (Goodbddy, 1966). In this case, differences in the arrangement of the oral tentacles may be responsible, although there might be some variation in the food content of the water since the species occupy somewhat different ecological niches. Little experimental work has been done on the nature and quantity of food required by ascidians, but Milkman (1967) maintained cultures of Botryllus schlosseri (Pallas) in sea water containing the centric diatom Cyclotellanana Hustedt at a concentration of 1-2 x 106 cells/ml. Apart from filter-feeders which accept a wide range of material suspended in the surrounding water, there is an ecological group of ascidians which appear habitually to take in bottom deposits. Amongst shallow-water species Styela coriacea Alder and Hancock is apparently a deposit-feeder (Diehl, 1957), but it is the small-bodied deep water species living on a soft muddy substratum which have most commonly developed this habit. The gut contents of these animals are similar to the surrounding sediment, and the small size of the body allows the oral siphon to draw in sediment from the loose interface of the substratum and water (Millar, 1970). I n these animals the gut was found to contain, in addition to inorganic material, small brown “cells ” and many bacteria. Those abyssal ascidians with a long stalk, such as Culeolus spp. may, however, live with the oral siphon some distance above the sediment, and their gut contents have been found to lack the bottom deposits common in sessile forms (Millar, 1959a). Although ascidians probably originated in shallow seas with a rich plankton and in consequence evolved the filter-feeding mechanism which most of them still possess, a number of species penetrated into deep water. Of these, a very few have abandoned the original feeding mechanism in favour of a quite different kind, adapted to taking larger organisms and bottom material. In Octacnemus Moseley, Hexacrobylus Sluiter and Gasterascidia Monniot and Monniot the perforated branchial aac is replaced by an unperforated tube or sac which is obviously incapable of filtering particles from a current of water. Instead, relatively large animals such as ostracods, nematodes, copepods and other crustaceans are taken (Ritter, 1906; Madsen, 1947; Millar, 1959a, 1970; Monniot and Monniot, 1968). These occur in the gut together with

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R. H. MILLAR

quantities of sediment, but whether the animals are captured alive and selectively, or merely engulfed along with the sediment is not known. The modifications to the oral siphon, which include enlargement and great muscular development, suggest active capture, but alternatively they could be adaptations for scooping up large quantities of bottom deposit (Millar, 1970). Nevertheless, Monniot and Monniot (1968) regard the structure of Gasterascidia sandersi Monniot and Monniot as adapted, not only to a predatory habit, but to movement over the substratum, an ability which may enable this ascidian to capture prey. One further problem which awaits investigation concerns the feeding habits of the curious interstitial ascidians described in a series of papers by C. and F. Monniot (see Monniot, 1966). Some of these species, which rarely exceed 3 mm in length, move amongst the sand grains of the substratum, and presumably feed on organic particles or organisms in the interstitial water. The branchial structure, although modified, is essentially similar t o that of filter-feeding ascidians.

111. BREEDING Reproduction in ascidians takes three forms : asexual reproduction by budding, which occurs only in some families ; fission of colonies, a process recorded in few species ; and sexual reproduction or breeding, which occurs universally throughout the group.

A. Breeding season

A number of methods can be used t o investigate the timing and duration of the breeding season. (i) Macroscopic or microscopic examination of specimens collected at intervals throughout the year shows the cyclic activity of ripening, filling and emptying of the gonads, and in certain species or populations only the presence of spent gonads in the samples indicates the onset of spawning (Millar, 1964a, 1960; Diehl, 1957) ; in other cases information of this kind complements studies by more direct methods. Establishing the period when animals have full gonads with ripe gametes does not, however, do more than define the period within which breeding may occur, given the appropriate stimulus, and species are known which have full gonads throughout the year, but which only breed successfully (judged by the settlement of larvae) in a more restricted period (Raja, 1963). Some workers have used artificial fertilization or spontaneous spawning of animals brought into the laboratory at intervals, t o provide a criterion of ripeness (Hirai and Tsubata, 1956; McDougall, 1943; Levine, 1962).

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THE BIOLOGY OF ASCIDIANS

(ii) Plankton samples give direct evidence of breeding, but in practice the method seldom has been used, owing to the difficulty of identifying ascidian larvae and to their brief appearance in the plankton, Brewin (1946), Lutzen (1960) and Dybern (1965) are amongst the few who have used plankton samples in this way, and the value of this approach is illustrated in Fig. 1which clearly shows the breeding season of a population of Ciona intestinalis in the Gullmar Fjord, Sweden (Dybern, 1965).

1959

1960

1961

FIG. 1. Seasonal occurrence of larvae of Ciona inhfinali.9 a t Stromnara, Sweden, as shown by the number of larvae per plankton scrmple (redrawn after Dybern, 1965).

(iii) The commonest approach has been that used in fouling studies ; test panels are placed in the sea at intervals and examined periodically for the presence of attached animals. Owing to the difficulty of identifying very young specimens, however, species are often recorded only some time after settlement, and in areas where growth is slow the breeding season may be considerably longer than that recorded. Another source of error arises from the requirement of certain species for a clean surface and others for an already fouled surface, before larval attachment will take place (Scheer, 1945; Goodbody, 1962), and the consequent doubt whether the absence of a species from test panels may have resulted from the unsuitable condition of the surface rather than from the absence of breeding. Any heavy mortality amongst the very young settled ascidians may also conceal the occurrence of breeding. (iv) Studies of size-distributions in natural populations may indicate the breeding period, by showing the appearance of new generations through the identification of peaks in the histograms (Allen, 1953;

8

R. € IKJLLAR I.

Diehl, 1957; Dybern, 1965,1969b ;Millar, 1952, 1954b, 1960 ;Sabbadin, 1955, 1957). Statistical analysis of size distribution in the adult populations, using the probability paper method (Harding, 1949 ; Cassie, 1950), should further refine estimates of the dates of larval settlement, but the method has not yet been used in ascidian studies. Temperature is generally recognized as a major factor controlling the sexual reproduction of marine invertebrates. Hutchins (1947), in discussing the bases for temperature zonation in geographical distribution in the sea, noted two situations in which temperature requirements will limit breeding : at the summer poleward boundary, beyond which the sea is too cold to permit breeding ; and at the winter equatorial boundary, beyond which it is too warm. Towards these geographical boundaries the timing and duration of the breeding season can be expected to show variations from the pattern prevailing over the main part of the range of a species. In only a few ascidian species is sufficient information available to test these ideas. The influence of temperature on the breeding season may be seen in Ciona intestinalis, a particularly favourable species since it occupies such a wide latitudinal range, and Dybern (1965) has summarized the observations of other workers (Berrill, 1935a; Orton, 1914, 1920; Millar, 1952; Sabbadin, 1957 ; Komarovsky and Schwartz, 1957 ; Millard, 1952 ; Runnstrclm, 1929, 1936) and added fresh evidence from Swedish populations. He showed that f. typica breeds during all or most of the year in the Mediterranean, and that the season is progressively restricted to the summer months towards the northern parts of its range. Runnstrclm (1927, 1929, 1936)had concluded that f. typicu is divided into a number of races each with its own breeding temperature characteristics, but Dybern doubts whether Runnstrclm’s experiments and hypothesis were sound. This, however, is a disagreement about genetic differentiation ; the controlling influence of temperature on the breeding season is not in dispute. Botryllw schlosseri is another species of wide distribution whose breeding season in a number of localities is known (Lo Bianco, 1909; Millar,1952 ;Sabbadin, 1955;L’Hardy, 1962 ; Polk, 1962). It is evident from Fig. 2 that the duration of breeding is progressively restricted, presumably by temperature, towards the cooler more northerly parts of the geographical range. An instance of the very restricted breeding season at the distributional limit of a species was investigated in Pelonuia corrwata Goodsir and Forbes (Millar, 1954a). At its southern boundary this boreo-arctic species breeds over a period of only 2-4 weeks in January and February, when the sea temperature is near its yearly minimum.

a

b

c

ti

E Go

Sea temperature, O C

F I ~2.. Geographical variation in the breeding season of Bolryllua echlosaeri (from data in L’Hardy, 1962 ; Lo Bianco, 1909 ; Miller, 1952 ; Polk, 1962 ; Sabbadin, 1955). Sea temperatures at a, Naples, b, Millport (Scotland) and c, Venice.

10

R. H. M I L T A R

SimilarlyStyela rustica (L.), a north polar species, breeds in January and February in the southern part of its range (Lutzen, 1960). Unfortunately in neither case is the breeding season known in more northerly areas.

%

%

25

.-..

FIG.3. Breeding of Dendrodoa groaaularia. Percentage of semplos with incubating Essex (England), embryos or larvae, in different size groups of adrdts. o----o,Millport (Scotland).Sea temperaturesat Essex, full line; and at Millport. broken linc.

Even over a comparatively short distance variations in the temperature regimes are reflected in the breeding cycle. Thus Dendrodoa grossularia (Van Beneden) in the Firth of Clyde breeds continuously from early summer until autumn with only a slight reduction in August, but in Esscx reproduction stops altogether for a short period in the summer (Fig. 3) (Millar, 1954b).

TEE BIOLOGY OF ASCIDIANS

OC

:-

Y

M

J

S

11

N

D l::[

.

.i

E

50

P

Fro. 4. Breeding of ascidiana on Scottish west coast, as shown by percentage of samples with incubating embryos (0-0) or larvae (.----a) (C-H, J, B). In A the condition of gonads indicated breeding. In B, I and L embryos and larvae are not represented separately. A, Pelonaiu corrugata; B, Dendrodoa groaaularia; C , Aplidium pailidurn; D, Sidnyum turbinatum; E, Aplidium nordmanni; F, A . punetum ; 0,Polydinum aurantium ; H, Didemnum candidum ; I Diploaoma lkkrianum ; J, Liaaodinum argylleme ; K, Clavelina lepadiformia ; L, Botryllua achloaaeri. Sea temperature in 1952, and in 1953. 0-0 (after Millar, 1958e).

.--..

In addition to examining the behaviour of one species in different places we may look for evidence of temperature effects by comparing the breeding seasons of several species in the same area, bearing in mind the position which each occupies within its total geographical range. Thus a group of species on the Scottish west coast shows a north boreoarctic species at the southern limit of its range breeding briefly in the winter, south boreo-arctic species breeding over a long period, and south boreal species with a short summer period (Fig. 4) (Millar, 1958a).

12

B. H. MILLAR

Amongst the ascidians of Asamushi, Japan, Hirai (1963) recorded some species as breeding in summer, and others only in autumn or winter and these restricted seasons may also relate to the position occupied by the species within their total distribution. In tropical waters a much longer reproductive season is possible. Goodbody (19 6 1 4 found that Ascidia nigra, Diplosoma macdonaldi Herdman and Symplegmu viride Herdman settled throughout the year in Kingston Harbour, Jamaica, although not at a uniform rate. Two of the species showed marked peaks, which did not, however, correlate obviously with variations in any environmental factor. As Goodbody noted, the peaks were of settlement and could have indicated greater larval survival rather than greater spawning activity. Prolonged breeding with an interruption in winter was found in a species-probably a Pyura-at Madras, India (Raja, 1963). Since the sea temperature in Madras harbour varies only between about 26°C and 29°C (Sebastian, 1953) other environmental factors may have imposed the seasonal cycle on reproduction, Elsewhere in warm waters Weiss (1948) observed a similar pattern of long but interrupted breeding in Botryllus planus (Van Name) and Botry1loh-h nigmm Herdman at Florida, U.S.A., and Didemnum candidum lutarium Van Name settled continuously but not uniformly. In warm seas with a marked seasonal temperature cycle ascidians may also breed throughout the year, with periods of greater and lesser intensity. Skerman (1959), in a study of fouling at Auckland, New Zealand, found at least four species which probably settle in every month. Here the mean annual range of sea temperature is about 11*7OC,but the temperature rarely falls below 11°C. It appears that in regions with a relatively high winter temperature, breeding is possible throughout the year, even when there is a large seasonal fluctuation in temperatures. Relatively little is known of the reproductive patterns of ascidians in polar seas, because of the difficulty of collecting in these regions throughout the year. Millar (1960) produced some evidence that subantarctic and antarctic species do not breed during the southern winter, and although larvae were present in specimens of Sycozoa sigillinoides Lesson collected in eight months of the year, it is not known how long they had been retained in the colonies or when they were released. Other compound species were found to have larvae during three or four summer months. In solitary species the evidence from the state of gonad development suggests a breeding period confined to the least cold months. Brewin (1946) studied ascidians from Portobello, New Zealand, and


13

concluded that species of the primitive families had a longer breeding season than those of more highly evolved families, but to generalize from these observations would require a closer examination, bearing in mind also the variation in season due to the location of species within their total ranges. Although water temperature largely controls breeding, the termination of the season does not appear to be closely related to a particular critical temperature. Several species in the Plymouth area cease breeding while the water is still warm and food supply ample for adult needs (Berrill, 1935b), and Dybern (1965) concluded that Ciona intestinalis stops spawning in autumn because of changes in the gonads brought about by falling temperature rather than by a critical temperature. There is some evidence, however, that gametes are not released until a certain temperature is reached (Huus, 1941) and that this is the temperature below which larval development is abnormal or impossible (Knaben, 1952). B. Spawning Spawning in oviparous forms appears generally to take place at a particular time of day and the resulting synchronization throughout a population will increase the chances of fertilization. Ciona intestinalis and Molgula manhattensis (De Kay) release eggs and sperm one to one and a half hours before sunrise (Castle, 1896; Conklin, 1905; Berrill, 1947a) and Corella parallelogramma (Miiller) (Huus, 1939), and Styela partita (Stimpson) do so in the late afternoon (Castle, 1896; Conklin, 1905; Rose, 1939). Hirai and Tsubata (1956) found that Halocynthia roretzi (Drasche) kept in the laboratory for a few days repeatedly spawned in the late morning. The mechanism controlling synchronous release of gametes in Corella parallelogramma depends on illumination following a period of darkness (Huus, 1939). Huus (1941) later suggested that a hormone may be involved. In Ciona intestinalis and Molgula manhattensis the gametes are shed approximately 4 and 24 minutes respectively after the animals are exposed to light, and the most effective light is of a wave-length 500-700 mp (Whittingham, 1967). Lambert and Brandt (1967) also studied the effect of light on the spawning of Ciona intestinalis, and after comparing the action spectrum for light-induced spawning with the absorption spectrum of cytochrome c, concluded that this or some other haemoprotein may be the receptor material. Although somewhat beyond the scope of the present review it is worth noting that many attempts have been made to discover whether

14

R. €I.

a functional relationship exists between the neural complex (ganglion and neural gland) and sexual activity and this work has been summarized by Dodd (1955) and by Hisaw et al. (1966). Despite conflicting experimental results and the discovery of neurosecretory cells in the ganglion (Dawson and Hisaw, 1964), it is at least doubtful if the neural complex is essential to the act of spawning, for Hisaw et al. noted normal gonad development and discharge of gametes in animals deprived of the complex for periods of up to a year. Nevertheless, the experiments of Sengel and Kieny (1962)) Sengel and Georges (1966) and Bouchard-Madrelle (1967) all strongly suggest that the neural complex has some influence on the development of the gonads and on spawning.

C. The larva 1. Development and release

Most solitary forms release their gametes into the sea, where fertilization and development take place, but almost all compound ascidians retain their eggs until the larva is complete and able to swim. A number of ways have been adopted of protecting the embryos during development, by retaining them within the oviduct, the atrial cavity or a brood pouch of the zooid, or in the test matrix of the colony. The most elaborate method yet discovered is in the New Zealand species Hypsist o mfasmerianu (Michaelsen)(Brewin, 1956a). In this species the ovary produces a single egg, only 25 p in diameter, which develops into a large larva in an oviducal brood pouch, there receiving nourishment through a pair of larval endodermal tubes. During the whole developmental period of 5& months, attachment to the parental zooid is maintained, and the resulting larva is very complex, with numerous buds. The advanced stage of development attained by the larva before release must be of considerable advantage in founding the new generation. A similar objective is achieved, in quite a different way, by the solitary Polycurpa tinctor (Quoy and Gaimard). Here the egg is very large (730 p in diameter) and rich in yolk, and develops within the atrial chamber directly into a miniature ascidian, without the intervention of a larval stage (Millar, 19628,). Larvae escape from the parent colony in various ways, according t o the site of incubation. I n most species the developing embryos are retained in the thorax and the larvae pass out directly through the atrial siphon where this opens on the surface of the colony, or via the common cloaca1 cavities. I n Euherdrnania claviformis Trason (1957) observed the passage of mature embryos from the oviduct to the atrium of the zooid, a process taking about 10 minutes, while the passage through the atrium lasted 3 4 5 0 minutes. Apparently the immature

THE BIOLOQY OF ASCIDIANS

16

larva was retained in the oviduct until in the final stages of development it had become narrow enough to pass the oviducal sphincter. Thoracic contractions, initiated by the presence of the tadpole in the base of the atrial cavity, then moved it forward and out through the siphon. A similar process may take place in Pycnoclavella stanleyi (Berrill and Abbott) (Trason, 1963). Levine (1962) observed some larvae of Eudistoma ritteri Van Name to leave the parent by active swimming and others to be carried out passively by the exhalent current, and in Metandrocarpa taylori the larvae may be expelled by vigorous contraction of the zooid (Abbott, 1955). In some genera, notably Distaplia and Sycozoa, the embryos and larvae are accommodated in an outgrowth of the thorax containing the terminal part of the oviduct. In Distaplia the brood pouch with its larvae becomes separated from the zooid which eventually dies and the colony then contains numerous isolated pouches. These are exposed and release their larvae when the common test of the colony disintegrates, following the disappearance of the zooids (Berrill, 1948a). The same process apparently occurs in Sywzoa (Millar, 1960), and in Synoicum adureanum (Herdman) (Kott, 1060) which is one of the few species of the family Polyclinidae in which larvae are not released through the atrial cavity. A somewhat different mechanism exists in those ascidians with a small zooid and a large egg which is unable to pass forward through the thorax. Here a single embryo generally develops at a time and as it grows, bulges from the zooid perhaps to be released by rupture of the body wall. Examples in the family Clavelinidae are Eudistoma digitatum Millar, E . vastum (Millar), and Distaplia durbanensis Millar (Millar, 1963, 1964a). In Botrylloides the tadpole breaks through the body wall to reach the common cloaca1 space (Berrill, 1947b). The family Didemnidae shows the greatest specialization in this direction, for the eggs pass downwards from the abdomen directly into the test of the colony, there to be fertilized and undergo their dcvelopment. An exception in the Didemnidae is Diplosomu cupuliferum (Kott), in which fertilization and development take place in the abdomen of the zooid (Lafargue, 1968). Release of didemnid larvae must involve partial or complete dissolution of the test matrix, and it is perhaps not surprising that they sometimes metamorphose while still within the colony (Millar, 1952). Kott (1969) has suggested that zooids are also produced from larvae retained in the colonies of the unrelated Synoicum adareanum and Distaplia cylindricu. There is some evidence that larvae, like gametes, may be released principally at certain times of day, since Grave and McCosh (1924)

16

It. H.BlILLAR

observed the larvae of Peropbra viridis (Verrill) being shed from colonies in the early morning, and there may be periodicity also in Botryllus schlosseri (Grave and Woodbridge, 1924). In Molgula citrina (Alder and Hancock), however, no definite period of release has been observed, under laboratory conditions (Grave, 1926),nor in Metandrocarpa taylori (Abbott, 1955). 2. Structure

Throughout the group many structural variations have appeared in the larva, as illustrated in Fig. 5 which shows the principal forms now known. We still have little idea, however, of the functional significance of the different kinds of adhesive papillae, anterior ampullae and epidermal vesicles which vary widely and have been used in interpreting the phylogeny of ascidians (Kott, 1969). The simplest type of larva, which probably represents the ancestral form, has an ovoid trunk with three conical adhesive papillae in a triangular arrangement, and no ampullae or epidermal vesicles. This form occurs in the Cionidae, Diazonidae, Ascidiidae, Corellidae, Pyuridae, Molgulidae and most of the solitary members of the Styelidae, and the larva is generally small, with a trunk from 0-15-0-30 mm in length. It is amongst the compound ascidians (families Clavelinidae, Polyclinidae, Didemnidae and subfamily Botryllinae) that the greatest modifications in larval structure have appeared. Here the papillae are usually borne on stalks, and often have a terminal cup with a central cone of secretory cells, but notable exceptions are the invaginated tubular papillae of Euherdmania (Trason, 1957; Millar, 1961a) (Fig. 5, no. 10) and Pycnoclavelh (Berrill, 1950; Trason, 1963) (Fig. 5 , no. 2) and the narrow elongated structures of Eudistoma fantasianum (Kott, 1957a) and E. digitatum (Millar, 1964a) (Fig. 5 , no. 8). The dual nature of the ascidian tadpole (Grave, 1935;Berrill, 1955; Millar, I966b), which serves the larval purposes of distribution and site selection and also carries the rudiments of the adult, has profoundly affected larval structure. Thus, amongst the compound forms, the rudimentary adult may already show small buds, or differentiated blastozooids as in Diplosoma (Fig. 5 , no. 17) and Polysyncraton magnilarvum (Millar, 196213) (Fig. 5, no. 16), or a sufficient set of blastozooids to constitute a small colony shortly after larval attachment, as in Hypsistozoa fasmerianu (Brewin, 1956a, 1959) (Fig. 5, no. 4). Larval size, too, is greatest amongst the compound forms. In many of these the larval trunk is 0.5-1.0 mm in length-considerably greater than the average size amongst the simple forms-and in a few it is much larger. Amongst the giants are the larvae of Polysyncraton magnilarvum at

FIQ.5. Types of ascidian larvae. Tho tail is not shown. The scale lines under the larvae show their relative sizes. 1, Clavelinu lepadiformia ; 2, Pycmclavdla atanleyi ; 3. Diatnpliu roaea ; 4, Hypaialoroafaamerkzna ; 5, s y w w a sigdlinoidea ; 6, Cyatodyles dellechinjei ; 7, Ewliatoma illolum ; 8 , Eudiatoma fanlasianum ; 9, Polycilor crystallinwr ; 10, Euherdmania claviformia ; 11, Peeudodiatoma arboreacena; 12, Aplidium nordmaiini; 13, Polyclinum auraniium ; 14, Symicum georgianum ; 15. Didemnum helgolandicum; 16, Polyayncrafan magnilanrum : 17, Diploaoma Iiaterknum ; 18. Diazona vwlacea ; 19, Tylobranehion apecioeum : 20, Cwna inteatinalia; 21, Aacidia rnentula; 22, Perophora lialeri; 23, Styela parlila; 24, Dendrodoa groasularia; 25, Dextrocarpa aolitaria; 26. Botrylloidea leachi ; 27, Pyura microcornus ; 28, Molgulo citrina (redrawn from authors mentioned in the text).

18

R. H. MILLAR

1.3 mm (Millar, 1962b), Eudistom fantasianum a t 1.5 mm (Kott, 1957a))Polyeitor circes a t 2.5 mm (Millar, 1963))Hypsistozoa fmmeriana at 2.5 mm (Brewin, 1956a, 1950)and Eudistomdigitatum a t 4 4 - 4 6 inm (Millar, 1964s). The functional significance of larval structure has been interpreted by Berrill (1955) in relation to the choice of a suitable site for adult life. Within the order Enterogona the large solitary forms live in places whcrc their small simple larva is adequate for site choice, but the compound forms have a more specialized habitat requiring a larger more efficient larva. Berrill traces a similar correspondence betwcen larval type and adult habitat through the families of the order Pleurogona. In particular the family Molgulidae shows an adaptive loss of the larval ocellus, for many molgulids live on sublittoral sand and mud, where larval reactions to changes in light intensity (shadow reflex) are unimportant or definitely disadvantageous. A further step has been taken by a number of the sand-dwelling molgulid species, by elimination of the larval stage, and the same adaptation has arisen independently in response to similar habitat requirements in the styelids Pelonaia corrugata Forbes and Goodsir (Millar, 1954a) and Polycarpa tinetor (Quoy and Gaimard) (Millar, 1962a). 2.0

1.60)

3

14-

a*

1.2-

0

W W

,a

1.0-

m

:.

B

-fl

c

0.8-

0.8-

rA 0.4-

0.2-

1

0!2

0!4

0!6

0!8

l!O

112

114

l!6

I

1.8

I

2.0

I

2.2

1

Tail length, m m FIG.6. Swimming s p e d in relation to size of larva (from data in Berrill, 1931).

19


3. Behaviour The ascidian larva has a characteristic pattern of behaviour, consisting of an initial period when it swims upwards (positive phototropism and negative geotropism) followed by a period when it swims or sinks downwards (Grave, 1920, 1926; Mast, 1921; Grave and Woodbridge, 1924 ; Sebastian, 1953). The initial phase serves to distribute larvae, and it is in the second phase that the critical reaction is elicited in response to a decrease in light. The larva then swims towards dark areas, which in nature tend to be the vertical or lower surfaces of rocks etc. At this time a large tailed larva is advantageous since it is able to turn, swim quickly and attach to the substratum (Berrill, 1955), and Berrill (1931) has shown that the larger the larva, the faster it swims

30-

.Q. CI

CI

I

0

0

1 I. . 0.1

0.2

0.3

0 I

04

. I

0.5

1

0.6

Diameter of egg. mm

Pra. 7. Relationship bctwecn longth of lerval life and size of egg, in various species. The vcrtical lincs indicate the range of larval life within a spocios, whom this is known (from data of authors mcntioncd in text).

The duration of free swimming life under laboratory conditions varies from a few minutes to several days, according to species. With the exception of a few in which the embryo is nourished from the parental zooid, large larvae develop only from large yolky eggs, and might be expected to have correspondingly long swimming periods. However, Fig. 7, based on information from several sources (Grave, 1921, 1935; Berrill, 1931, 1935a, 1947b, 1948a, b, c, 1950; Millar, 1951, 1954b; Brewin, 1959; Sebastian, 1953, 1954) shows no strict relationship between larval duration and egg size (taken as a measure of larval A.X.B.--8

2

20

R. H. MLLdR

size). But since the larval yolk remains largely unused, to be carried over into the adult stage (Berrill, 1950), the energy available to the larva to maintain its swimming bears little relation to the amount of visible yolk. There is also considerable variation in the larval period within species (Fig. 8) (Grave, 1920, 1822, 102G; Gravc and McCosh, 1924; Grave and Nicoll, 1940; Grave and Woodbridgc, 1024; Cloney, 1961; Levine, 1962). Grave and Woodbridge (1024) considered whether the wide differences in Botrgllus might have a gcnctic basis, but found no morphological evidence of this in thc resulting colonies. If the phenomenon also occurs in nature i t may ensure that some larvae settle near the parents whereas others, more widely dispersed, eiiablc the spccics to explore more distant habitats. Lambert ( 1968) recorded considerable a

.a

9

10

Hours Fro. 8. Range of larval life within species. a, Molgula cifrina (redrawn from Grave, 1926); b, Eolryllus achloaaeri (redrawn from Grave and Wooclbritlgc, 1924); c, Perop h o m viridia (rodrawn from Grave and McCosh, 1924).

local settlement of Corella willmeriana Herdman when the population was large, and the inference is that many larvae settled quite soon after hatching. Polk (1962) made a similar observation on Botryllus schlosseri in a dock at Ostend, where larval settlement was dense near the parent stocks but sparse only 1 km away. These events could also result from gregarious settling behaviour (see p. 48). 4. Settlement

At the end of its free swimming phase the larva becomes attached to the substratum and metamorphoses, but in spite of many studies (see Berrill, 1950 ; Lynch, 1961), the controlling factors are not understood. Various substances which have been found to induce fixation include tissue extracts (Grave, 1935) and copper (Glaser and Anslow, 1949), but the experiments of Whittaker (1964) cast doubt on the role of copper. Experimental results in any case must be applied with caution to

TEE BIOLOGY OF ASCIDIAXS

21

natural conditions and do little more than suggest some possibilities. Grave (1935) believed, however, that a metabolic product of swimming activity is essential for metamorphosis. Nevertheless, larvae irnmobilized by narcotization will metamorphose at about the same time as free swimming controls (Bell, 1955), and although metabolic products may be concerned, their effect does not appear to be related in a simple way to the muscular activity of the larva. Fixation to the substratum is not always essential for metamorphosis; Cloney (1961) for instance found that, although most larvae of Boltenia villosa (Stimpson) in a culture attach before metamorphosing, others do not. The larvae of Eudistomu ritteri Van Name also vary in this respect (Lcvine, 1962), and Carlisle (1961) reported postmetamorphic stages of Diplosomu listerianum (Milne Edwards) and Cionu intestinalis in the plankton of the Plymouth aquarium. It may be usual for a proportion of the larvae, failing to contact a solid object, to metamorphose while still planktonic and subsequently to become attached. Ciona retains the ability to fix itself even as an adult (Berrill, 1929; Millar, 1953a). Before fixation takes place the larval papillae become sticky and in some species this precedes contact with the substratum. Thus in Perophora viridis a drop of viscid material is secreted by each papilla towards the end of the free-swimmingperiod and attachment follows contact with a solid surface (Grave and McCosh, 1924). In Eudistomu ritteri the papillae are already in an everted condition while the larva is swimming (Levine, 1962). Rapid eversion of the papillae, with exposure of the adhesive surface, precedes attachment in Euherdmunia claviformis (Ritter) (Trason, 1957) and in Pycnoclavella stanleyi (Berrill and Abbott) (Trason, 1963). Trason (1963) believed that a band of circular muscles in the larval trunk of E . claviformis may cause eversion of the papillae. Although the family Polyclinidae have a different kind of papilla, consisting of a goblet containing central secretory cells, extrusion is also effected by deformation of the papilla, which forces out the secretory cells and the secretion (Grave, 1920; Sebastian, 1954). In this case the mechanism is unknown, for there do not appear to be muscles in the papillae. Very little is known regarding the choice of substratum by the larva, or indeed if much choice is exercised. The presence of nerve fibres in the adhesive papillae of botryllid larvae (Grave, 1934) suggests that some response is made, presumably on contact with solid surfaces, but there is nothing to indicate whether surfaces are tested until a suitable one is found for attachment. Goodbody (1963a) believed that larvae of Ascidia nigra may be attracted to iron, since unpainted iron develops a dense growth of the species. It is possible, however, that observed

22

R. H. MlLLAR

differences in population densities may have resulted from variations in thc surface texture rather than from differential settlement, since

texture may affect the security of attached larvae and young stages. Nevertheless, he also observed that, while larvae of A . nigra will settle on almost any clean surface, those of A. interrupta Heller apparently require a degree of fouling on the substratum before they will settle. There is scope for experiment and observation in this field to show whether the physical and chemical nature of the surface is important or whether, as Dybern (1963)found in Cionu,the requirement is simply for a site with generally adequate conditions for adult life. 5. Evolution

Many authors have discussed the origin of the tadpole larva in relation to the ancestry of the vertebrates, but little fresh evidence has appeared recently. Both Berrill(l955) and Millar (1966b)take the view that this particular larval form arose within the tunicates. An elongated muscular body may have been a consequence of the loss of external ciliation due to the development of test. Jefferies (1968), however, believes that the tadpole may indicate the line of descent from Cambrian members of the subphylum Calcichordata (Jefferies, 1967), a view implying that the ancestral tunicates were free-swimming animal8 which later adopted a sessile habit for the adult while retaining a pelagic larva. Whatever may be the significance of the ascidian tadpole in this context, the striking similarity in the fine structure of the larval ocellus and the vertebrate eye (Dilly, 1961)can scarcely be a coincidence or the result of convergent evolution.

IV. LIFE CYCLE:GROWTH,SUCCESSION OF GENERATIONSAND MORTALITY The life cycle of solitary ascidians is relatively simple, and can be analysed as the establishment of the new individual, its growth, breeding and death; and appropriate measurements can be made at each stage. In compound forms asexual reproduction introduces a complication, and the resulting colony is to be regarded as the biological unit. It undergoes a complex series of changes involving various degrees of decay, renewal and, occasionally, division. Increase in body length has been used almost universally as a measure of growth in simple ascidians, and although filr from ideal, since the rclationship between length and weight is rarely known, it does givc a useful index. Practical difficulties arise because the body in most species is attached to a solid object which may interfere with easy and accurate measurement, and the habit of contracting when disturbed

23


further reduces accuracy. Most growth studies have been made by measurements in successive samples of a population, and in only a few cmes have individuals been followed. That the two methods give sufficiently similar results is indicated by population studies on Ciona intestinalis in a Scottish harbour (Millar, 1952) and growth rates obtained by measurements of marked individuals in an aquarium on the same coast (Millar, 1953a) (Fig. 9). The pattern is a simple one. Animals settle in the summer, make only limited growth in that year, stop growing in winter, and quickly grow to full size in the following spring and summer. But in other areas the timing of events is different, 121

I

.I

I

I " M ' A

' M ' J

' J

'

A

'

H

'

o

'

N

'

~

'

Fro. 9. Growth of Cionn intestinalis. Each line represents the body length ofan individual in a population in aquarium tanks at Millport. The black circles are the mean body lengths in samples of a population in a nearby dock (redrawn from Miller, 1953a and from data in Miller, 1952).

and, fortunately, this widespread species has been studied in a number of places where the prevailing conditions, and in particular the temperature regime, vary considerably. Dybern (1965) has reviewed the results and concludes that there is " a clear relation between age, growth, spawning and embryonic development, on the one hand, and the environmental temperature conditions, on the other ". Since sexual maturity is at least partly related to body size (Millar, 1952),the growth rate affects the timing of spawnings in the season a d . consequently the succession of generations. Table I, taken from Dybern (1965), summarizes the results of numerous workers (RunnstrBm, 1927, 1936; Berrill, 1935a; Orton, 1914, 1920; Millar, 1952; Sabbadin, 1957; Komarovsky and Schwartz, 1957; Millard, 1952; Pbrhs, 1952;Lo Bianco, 1909 ;Scheer, 1945). The population structure vanes markedly through-

TABLEI. SUMMARYOF

Temperature

hTo.of generations per year

Main spawning periods

0 to 500 m

Kf, a hyperbolic relationship would exist between the specific growth rate and the cellular nutrient content. The intercept corresponding t o zero growth rate represents the minimum cellular nutrient content which will permit cell division t o continue. Typical values for this (all in pmoles/cell) are: for nitratelimited growth, 3.1 x 10-8 (Isochrysisgalbana; Caperon, 1968) and for (Phaeodactylum tricornutum ; phosphate-limited growth, 2 x

124

E. D. S. CORNER AND ANTHONY Q. DAVIES I

I

I

I

I

1

FIQ.4. This illustrates how the relationship between the specific growth rate, p, and the cellular nutrient content, Q, depends upon the rclative magnitudes of the halfsaturation constants for nutrient uptake, K", and for growth, K:. p was assumed to vary with the nutrient concentration in the medium, S, according to the equation p = p,S/(K: 6 )where pm= 0.02 h-' and K : = 10 pM. The equation used for the rate of uptake was V = V,S/(K: $- S)with (A)Vm= 1 h - ' and K: = 1 pM, (here V, is expressed as the rate of doubling of the cellular nutrient content); (B)Ym= 1 h-' and K : = 2 p M ; and ( C ) V , = 1 h-' and K : = 6 pM. Only when K: = K : is the value of p independent of Q ; for KP, > K:, a hyperbolic relationship between p and Q results. (After Eppley and Thomas, 1969.)

+

Kuenzler and Ketchum, 1962), 5 x (Asterionella juponim; Goldberg et al., 1951), 1-05 x for Cylindrotheca closterium and 1.04 x for Cyclotella nunu Hustedt (Carpenter, 1970). The phosphate-dependent growth of Chaetoceros gracile appears to fall into neither of the previously described categories, the growth rate increasing approximately linearly with the phosphate concentration in the medium up to about 0.23 wg-atoms PO$-P/l, above which it remains practically constant (Thomas and Dodson, 1968). Eppley and Thomas ( 1969) take this to indicate that the rate of phosphate uptake limits growth at low phosphate concentrations, so that the growth rate at first increases hyperbolically ; but at higher concentrations, the growth rate reaches its maximum value. The potential application of half-saturation constants to the explanation of phytoplankton succession has been well illustrated by Eppley et al. (1969b). By assuming that values of K: are the same as their measured values of K:, they calculated how the specific growth rates of four phytoplankton species would vary with the available nitrate and ammonia concentrations (Fig. 5 ) . The data, show that at low nutrient

PLANKTON IN NITROQEN AND PHOSPHORUS OY-S

126

NH; concentration (pM1

FIQ.6. Calculated specific growth rates of four marine phytoplankton species as a function of (A) nitrate and (B) ammonium concentration. The growth rates correspond to an irradiance level of 20% of that due to sunlight at the sea surface. a = Coccolithw huxleyi. b = Dilylum brightwellii. c = Skeletimema coatalum and d = Dunaliella tertiolecta. (After Eppley et al., 1969b.)

levels the growth of Coccolithus huxleyi (Lohm.) Kampt would be favoured ; whereas at higher levels, the diatoms would predominate. Changes in the phytoplankton in accord with this have actually been observed off southern California where upwelling can increase the nitrate level of the surface waters (R. W. Eppley, unpublished data).

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E. D. S. CORNER AND ANTHONY 0. DAMES

The euryhaline species Dunaliella tertiolecta would be expected to compete successfully only when ammonia is available, the other three species presumably being excluded, by their lack of salinity tolerance, from the rock pools where Dunaliella is usually found. Should the easily measured half-saturation constant for nutrient uptake prove to be of general use for predicting the growth of phytoplankton, it is likely that many of the outstanding problems relating t o phytoplankton distribution could be explained. A great deal more research in this field is obviously required.

VII. NITROQEN AND PHOSPHORUS LEVELSIN PHYTOPLANKTON There is surprisingly little published information on nitrogen and phosphorus levels in natural populations of marine phytoplankton. The most detailed study remains that of Harris and Riley (1956) who followed the changes in the chemical and species composition of the phytoplankton in Long Island Sound over a period of a year. Their data are reproduced in Table I (Section 111). Between March and June, approximate doubling of the nitrogen and phosphorus contents took place and was associated with the change from Skeletonem costatum, as the dominant species, to the presence of substantial numbers of dinoflagellates: a small decrease in the nitrogen :phosphorus ratio also occurred. The change in the species composition probably resulted from depletion of the available nitrate in March (Riley and Conover, 1956), for McAllister et al. (1961) noted in their large-scale cultures of natural, coastal phytoplankton populations that the dinoflagellates increased only after the nitrates had been completely utilized (although in this case their presence appeared to cause an increase in the nitrogen : phosphorus ratio in the phytoplankton). Parsons et al. (1961) have provided data on the chemical composition of 11 species of marine phytoplankton grown in culture, and their results for nitrogen and phosphorus content are given in Table I1 (Section 111). Both elements were present in greater amounts in the cultured phytoplankton than they were in the natural populations examined by Harris and Riley; and, as mentioned earlier (see p. 112) the nitrogen : phosphorus ratios varied considerably between species, usually being much smaller than the accepted value of 16 :1. Although the higher concentrations of nutrients available in the cultures of Parsons et al. (500 pg-atoms NO;-N/l; 50 pg-atoms PO;--P/l) may have been the cause of the higher nitrogen and phosphorus levels in the phytoplankton, it should be noted that Strickland et al. (1969) found that the nitrogen and phosphorus contents of cells grown in large-scale cultures under near natural conditions were not

127

PLANKTON IN NITROGEN AND PHOSPHORUS CYCLES

greatly dependent on either the level or the nature of the nitrogen aupply that was utilized (Table V). Moreover, laboratory-cultured cells of Ditylum brightwellii contained less nitrogen and phosphorus than did those from the deep-tank cultures. TABLEV. THE CELLULARNITROGEN AND PHOSPHORUS CONTENTSAND N :P RATIOS OF Two PHYTOPLANKTONIC SPECIES IN RELATION TO THE NUTRIENT SUPPLY. ( D a t a from Strickland et d.,1969.) Ditylum brightwellii Deep-tank culture (14.5"C) 0.9 pg-atoms NH:-N/I

Laboratory culture (2OOC) 260 pgatoms NO;-N/l

NH -grown cells NO J -grown cells . . -. - -. -

__ Nitrogen (pgleell) Phosphorus (pglcell) N: P (atoms)

300 65 10.2 :1

120 23

320 80 8.8: 1

1143:l

Caehonina tiiei ~-

-

-

__ _

_ _.__ ~ -

-

-

-

Deep-tank culture (2OOC)

NH: -grown cells

I

I

Nitrogen (pglcell) Phosphorus (pgleell) N: P (atoms)

Nutrient-starved cells

24.5 6.7 8-1 :I

94:l

NO -grown cells

'

-

--

-~

34.0 7.2 10*6:1

The relationship, if there be one, between the nitrogen and phosphorus contents of marine phytoplankton and their nutrient supply remains obscure.

A. Release of organic forms of nitrogen and phosphorw by phytoplanktm A considerable proportion of the organic matter produced during photosynthesis by phytoplankton may be released in a soluble form by

128

E. D. 9. CORNER AND ANTHONY

a. DAVIES

actively growing populations. For example, Antia et al. (1963) found that 35% of the carbon fixed in a large-scale culture of coastal phytoplankton, growing under near natural conditions, reappeared in the sea water. Some of this released material undoubtedly consists of compounds of nitrogen and phosphorus: thus, on several occasions it has been observed that the levels of the organic forms of these elements increase as a result of phytoplankton growth under natural conditions (Strickland and Austin, 1960 ; Ketchum and Corwin, 1965), as well as in large-scale cultures of natural populations (McAllister et ul., 1961 ; Antia et al., 1963) and of single species (Strickland et al., 1969).

Dissolved organic nitrogen appears to be released mainly in the form of proteins and amino acids (Hellebust, 1965) and the release of amino acids by nitrogen-fixing blue-green algae may be of significance in the marine nitrogen cycle (Stewart, 1963). The nature of the organic phosphorus released has not yet been elucidated; but it is likely t o contain monophosphate esters (Kuenzler, 1970). Kuenzler has recently shown that the dissolved organic phosphorus (DOP) in cultures of marine phytoplankton reaches a maximum level just when the cultures are entering the stationary phase ; and corresponds to between 12 and 26% of the total phosphorus present. I n the case of Cyclotella cryptica Reimann, Lewin and Guiilard, the DOP thus formed is reassimilated during the stationary phase; but with other species, such as Thulassiosiru juviatilis Hustedt and Dunuliella tertiolecta, the level of DOP increased with the age of the culture. The assimilation by phytoplankton of the DOP produced by different species was also demonstrated, and the fraction taken up was found to vary with species. Thus, Dunaliella tertiolecta and Synechococcus sp. took up the smallest amounts, probably because these species do not themselves produce external phosphatases. Kuenzler makes the interesting point that DOP released by phytoplankton in the euphotic zone may be as important as that excreted by zooplankton ; and that relative abilities to utilize this organic phosphate could provide some species with a competitive advantage over others.

VIII. THEASSIMILATION OF NITROGEN AND PHOSPHORUS BY ZOOPLANKTON

This section is the first of several dealing with the part played by zooplankton in the turnover of nitrogen and phosphorus in the sea ;and begins with a brief account of the possible dietary sources of nitrogen and phosphorus available t o the animals.


129

A. Living diets Numerous laboratory studies have shown that many unicellular algae are used as foods by zooplanktonic animals (see reviews by Marshall and Orr, 1962; Corner and Cowey, 1964, 1968). In addition, an inverse relationship has been found between the relative quantities of zooplankton and phytoplankton in a number of sea areas, ranging from Antarctic waters (Hardy and Gunther, 1935) t o sub-tropical regions such as the coast of Bermuda (Beers and Herman, 1969; Herman and Beers, 1969 ; Station " A ", March 196PMarch 1965) : other areas, with which we shall be dealing in some detail, are the English Channel (Harvey et al., 1935), Long Island Sound (Riley and Bumpus, 1946) and Narragansett Bay (Martin, 1965). The nutritive value of algal diets has been established by studies in which animals such as Tigriopus californicus (Baker) (Provasoli et al., 1959), Euterpina mutifrom (Dana) (Neunes and Pongolini, 1965) and Acartia tonsa Dana (Zillioux and Wilson, 1966) have been reared through several generations on plant diets. No single species of alga can support an indefinite number of generations, however, because apparently none can supply optimal amounts of all the essential micronutrients. It has long been known that certain phyla of the zooplankton, notably the chaetognaths, cnidarians and ctenophores are carnivores; and this kind of feeding is now also recognized as characteristic of certain copepods. Thus, Anraku and Omori (1963) found that Centropages humatus (Lilljeborg) would eat nauplii of Artemia salina (L.) as well as the diatom Thulmsiosira jluviatilis Hustedt, and that Tortanus diemudatus (Thompson and Scott) ate only animal food, including other copepods such as Temoralongicornis (Miiller)and PseucEocalanus minutus (Krsyer). A further example is Euphausia pmifica Hansen, which reduces its feeding on diatoms when Artemia nauplii are present, preferring the latter as a food (Lasker, 1966). Similarly, Mullin (1966), investigating 19 species of copepod from the Indian Ocean, found that all consumed animal food at least as readily as they fed on phytoplankton, and several preferred animal food only. The nutritive value of animal diets has been demonstrated by Lasker and Theilacker (1965) who reared three species of euphausiid on a diet of Artemia nauplii alone ; and that of a mixed animal and plant diet established by Mullin and Brooks (1967) who reared Rhincalanwr wutus Giesbrecht using Artemia as a dietary supplement for the later copepodite stages.

130

E. D. 5. CORNER AND ANTHONY 0 . DAVIES

B. Detritus This fraction of the particulate material in the sea contains no living plants or animals but includes bacteria, the faecal pellets and cast moults of zooplankton and disintegrated phytoplankton cells. Its capture by zooplankton has been deduced from examination of gut contents. For example, Macdonald (1927) found that the guts of small specimens of Meganyctiphanes norvegica (M. Sars) contained both diatoms and wet dust ”, i.e. flocculent detritus ; and Mauchlinc (1960) found 20% by volume of “ grit ” and vegetable detritus in the guts of Calanus jinmarchicus (Gunnerus) from deep water (150 m) in the same sea area. If detritus were a valuable diet for zooplankton, a large source of food would be available to the animals, for Jsrgensen (1966) concludes that of the total particulate material present in the sea generally only 10-20% by weight is represented by phytoplankton. However, the nutritive value of detritus is by no means well established. Thus, so far the only “ natural ” detritus tested is that obtained by Baylor and Sutcliffe (1963), using material extracted from sea water by the action of rising bubbles. The test animal was Artemia salina and the growth rate of animals fed on detritus was compared with that of controls either starved or fed on yeast. For the first four days animals given detritus or yeast as a food had roughly the same growth rate, after which that of animals fed on detritus was lower, although they continued to increase in size until the end of the sixteenth day. No measurements were made of the relative levels of the two diets, however, and to establish the presence of dietary factors needed for reproduction would require a much longer study, including attempts to rear the animals through several generations. Moreover, Paffenhtifer and Strickland (1970), studying an animal more representative of marine zooplankton, found that natural detritus is not eaten by Calanus helgolandicus (Claus), although the animal will apparently eat disintegrated samples of its own faecal pellets, as well as “ dead ’’ diatom cells. It would be interesting to know whether these two ingested forms of detritus have any nutritive value. I‘

C . Dissolved organic material Putter (1909) was the first t o claim that organic substances dissolved in sea water may be absorbed and used by animals directly. However, it has since become clear, mainly through the work of Moore et al. (1912) and Krogh (1931), that the methods originally used by Putter led to greatly overestimated levels of dissolved organic material. Never-

PLANKTON I N NITROOEN A N D PHOSPHORUS CYCLES

131

theless, renewed interest in Putter’s hypothesis has been stimulated by a series of studies by Stephens and co-workers, summarized by Stephens (1968), which have shown that a largc number of marine animals, representing many different phyla, are able t o remove organic substances, including nitrogenous compounds such as amino acids, from low concentrations in sea water. Most of the findings were made with soft-bodied animals ; but McWhinnie and Johanneck (1 966) have briefly described evidence consistent with the view that the Antarctic euphausiid Euphausia tricccantha Holt and Tattersall can absorb certain organic compounds directly from sea water. Concerning nitrogenous substances, Corner and Cowey ( 1964) have emphasized that the uptake of amino acids by zooplankton from sea water would have t o take place against a high concentration gradient and therefore involve considerable metabolic work. They drew attcntion t o the presence of a relatively large concentration of free amino acids in the tissues of Calanus finmarchicus, the quantity accounting for 1620% of the protein content of the animal (Cowey and Corner, 1963a). Furthcr evidence for the presence of high concentrations of free amino acids in zooplankton has been found by Jeffries (1969) using Acurtia clausi Giesbrecht and A . toma. The total amount of free amino acids in CalanusJinmarchicus was 2.45 mg N/g wet weight ; and assuming a wet weight : dry weight ratio of 6 :1 , this would mean that the concentration of amino-acid N present in the tissue fluids was roughly 3 mg/ml. So far, analyses of the levels of amino acids dissolved in sea water have given values of only 2-1 6 pg amino acid11 (Chau and Riley, 1966). Accordingly, these substances would have t o be transported against a concentration gradient of 10s-107: I . However, Stephens (1968) calculates that for an amino acid such as glycine the work involved in moving against a high concentration gradient represents only a small fraction of the energy derivable by oxidation of the molecule. He also estimates that the fraction of metabolic energy required t o account for the accumulation of amino acids is not likely t o be more than 3-4% under natural conditions, and the process is thcrcfore “ energetically possible ”. On the other hand, Johannes et ul. (1969) claim that the removal of radioactively labelled organic compounds from solution by marine invertebrates does not constitute proof of net uptake of these substances, for none of the studies made previously involved measurement of the total release rates of these compounds by the animals. According to Johannes et ul. (1969) there is, in fact, more likely t o be a net loss than a net gain of organic substances, such as amino acids, by marine invertebrates.

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E. D. 9. CORNER AND ANTHONY 0.DAVIES

Concerning zooplankton, Jargensen (1966) has expressed the view that the well-developed feeding mechanisms of these animals are consistent with the importance of particulate material as a source of food. Jarrgcnsen (1966) also makes the important point that the use of either detritus or dissolved material as a principal food by zooplankton is inconsistent with the view that grazing is an important factor in controlling the size of the phytoplankton population in the sea.

D. Laboratory studies on assimilation Harvey et al. (1935) observed that large numbers of faecal pellets were produced by zooplankton when feeding on phytoplankton in the English Channel during spring. Undigested plant cells were detected in the contents of the faecal pellets, and this led to the view that the plant food present in a diatom bloom might be poorly digested. Twenty years were to pass before this problem was examined in the laboratory, t,he first definitive study being made by Marshall and Orr (1955a) using the copepod C. jinmarchicus. In Calanus, digestion takes place in the wide anterior part of the gut. As the food passes into the narrow posterior end it is gradually compacted into a faecal pellet which is subsequently ejected, enclosed in a pellicle that is probably chitinous. Marshall and Orr (1955s) cultured a number of diatoms and phytoflagellates in media containing radioactive phosphorus and fed the [32P]-labelIed plants t o the animal. Feeding took place in the dark and the experimental vessels were slowly rotated in a vertical plane so that the plant food would not settle out. After about 21 h, the animals, eggs and faecal pellets were removed and measured for radioactivity. The sum of the quantities of 3aP in these three fractions was assumed to give the total 32Pingested ; and the amount in the faecal pellets, when subtracted from this total, gave the quantity of 32Pdigested. This latter quantity, expressed as a percentage of the former, gave the assimilation efficiency-that is, the percentage of ingested food digested and absorbed. It should be noted that the experimental technique was such that any small amount of 32Pretained in the gut of the animal would have been estimated as part of the assimilated fraction and not as potential faecal material. This may have led to a slight over-estimate of assimilation efficiency. On the other hand, apart from faecal pellets the animal also excretes soluble products of metabolism. To measure this soluble excretion Marshall and Orr (1955a) fed Calanus on a rich culture of [32P)-lrcbelledalgae for about one week, then transferred the animals to fresh sea water and estimated the fall in level of 32Pin the bodies over several weeks. They found that, compared with living


133

Calanus, dead animals lost 32Pat a much faster rate and they regarded the repeated handling of the animals during the excretion experiments as probably leading to an over-estimate of the amount of 32Plost. In addition, they doubted that 32Pnewly acquired from the labelled plant food was in equilibrium throughout the bodies of the animals and thought that it might be preferentially excreted. Accordingly, they regarded the excretion of 32P as probably rather low and did not include it as part of the total quantity originally ingested by the animals. As a consequence,this led to a slight underestimate of assimilation efficiency. The actual values found were much higher than expected. Thus, of four species of diatom tested, the percentage assimilation was always over 50% and usually over 80%. Moreover, this percentage did not sensibly change with the concentration of food organism. Nine species of flagellate were also used, and again assimilation efficiencies were generally high. For example, in a series of experiments involving a range of concentrations of Cricosphaera elongata (Droop) Braarud (as Syracosphaera ebngata Droop) assimilation efficiency was always greater than 90%. Similar results were obtained with six species of dinoflagellate. A particularly striking observation was that Calanus feeding on rich cultures of Chaetoceros decipiens Cleve produced a faecal pellet every 5-7 min, yet even in these circumstances 86% of the food was assimilated. By rough dissection of the Calanus after feeding with labelled cultures it was possible t o see the approximate distribution of the absorbed 32Pthroughout the body. It is interesting to note that a large quantity was found in the fat in the pre-adult stage V and in males, whereas in females-which normally do not contain a fat-reserve-it was present largely in the reproductive system. One criticism that might be made of these findings, and one fully recognized by the authors, is that they refer only t o the phosphoruscontaining part of the food and may not apply to other dietary constituents. However, the results of other experiments by Marshall and Orr (1955b), using cultures labelled with 14C instead of 32P, generally confirmed those obtained in the earlier study. Thus, in experiments with the flagellate Cryptomonas sp., assimilation efficiency ranged from 53-78%, compared with 51439% in cultures labelled with 32P.Similarly, the values obtained in experiments with the diatom Skeletonema eostatum were 60-75%, compared with those of 54~5437.0%found in the earlier study. Marshall and Orr (1956) obtained data for phosphorus assimilation using the younger stages of CalanusJinmarchicus. They found, as in the case of adults, that the animals showed high assimilation efficiencies.

134


Thus, with Ditylum as a diet, late naupliar and young copepodite stages assimilated 77.8-95.9y0 of the food ; with Syracosphuera (Criwsphuera), assimilation was consistently higher than 98% ; and copepodite I, feeding on Skeletonema, assimilated 48.9-91.5%. Berner (1962), studying feeding by the copepod Temora longicornis (Miiller), also found high assimilation efficiencies, the animals assimilating 52.0-97-5% (average 77 yo) of a diet of [3aP]-labelled Skeletonema cells. Because carbon and phosphorus are important constituents of the algal cell, Marshall and Om (1955a) concluded that the major part of the organic material ingested by Calanus was assimilated. It would be unreasonable, however, to expect every dietary constituent to be assimilated with the same high efficiency ; and lower values have been obtained for the assimilation of nitrogen, studied by Corner et al. (1967) using Skeletonema as the test diet. The level of particulate nitrogen available to the animals at the start of a feeding experiment was determined by chemical analysis and compared with the quantity remaining after the animals had fed on the culture for 24 h. The difference between the two levels gave the quantity of nitrogen removed by the animals. Faecal pellets produced during the experimental period were collected and analysed for nitrogen to obtain the quantity unassimilated. The amount of nitrogen assimilated was estimated by subtracting the quantity present as faecal pellets from the total amount removed by the animals, and the value so obtained, when expressed as a percentage of the total amount removed, gave the assimilation efficiency. The values found, with Skeletonema used at concentrations representing 35-270 pg particulate N/1, were in the range 57-5-67.5% and, as found by Marshall and Om (1955a) in their experiments with 32P,there was no correlation between the level of available food and the proportion assimilated. This method, like that of Marshall and Orr (1955a), included the quantitative collection of faecal pellets ; and the separation of these from uneaten plant cells and eggs is always difficult and laborious. I n addition, Corner et al. (1967) found that in studies using Brachiomonas submarina Bohlin and Criwsphuera as plant foods the level of particulate nitrogen increased during the feeding experiments, in spite of grazing by the animals (as demonstrated by the production of faecal pellets). A possible cause of this increase may have been that soluble products excreted by the animals encouraged cell division by the plants. However, it is difficult to understand why this should have influenced the results obtained in experiments with Brachiomonas and Criwsphuera, but not those found using Skeletonema.


135

A " ratio " method for estimating assimilation efficiency, described by Conover (1966a), has the great advantage that the quantitative collection of faecal pellets is unnecessary. The method depends on the assumption that only the organic component of the food is significantly altered by the digestion process ; hence, it is only necessary to obtain the ratio ash-free dry weight : dry weight for a sample of the food and a sample of the faeces to calculate the percentage assimilation of the organic fraction. Conover used the method to estimate assimilation efficiency in terms of the total amounts of organic material in the diet. However, it could also be used to measure assimilation in terms of particular dietary components, such as phosphorus, for percentage assimilation can be expressed in terms of the ratio [organic P : total PI in the food and in the faecal pellets. Total P could be determined by digesting the sample with concentrated sulphuric acid and estimating the inorganic phosphate so formed using a standard method (e.g. that of Murphy and Riley, 1962). Organic P would then be estimated as the difference between this total value and the quantity of soluble inorganic phosphate alone. Conover (1966b) used the " ratio " method to study the assimilation efficiency of Calanus hyperboreus K r ~ y e rfeeding on Thulassiosira jluviatilis, and found that there was no significant correlation between percentage assimilation and either the food level or the quantity of food ingested. Thus, the average value for assimilation remained close to 70% for a range of food concentrations representing 100 to 1 900 pg C/1, the latter level being about three times the maximum concentration found at the peak of the spring bloom in the Gulf of Maine. Conover also applied the method in further experiments, carried out at sea, and found that mixed zooplankton feeding on natural particulate material assimilated, on average, 67% of the ingested food. Conover (1966a, b) makes clear that the accurate determination of assimilation by the method depends upon organic matter and ash being ingested by zooplankton in the same proportions as they occur in the natural food of the animals. This will not happen, however, if the food is destroyed during capture and the contents spilled ; or if the animal, when feeding on particulate material, selects the organic fraction of the diet in preference to the inorganic fraction. Evidence that such selection may occur has been obtained in experiments with Calanus helgolandicus by Corner (1961). However, these animals were collected from a coastal area where much of the unselected inorganic material could have been terrigenous. Conover (1966a) found that in areas away from the coast, estimations of assimilation with natural particulate

136

E. D. 8 . CORNER AND ANTHONY 0 . DAVIES

material as the food were usually comparable to laboratory measurements with unialgal diets. Direct experimental verification of the basic assumption that inorganic material is not assimilated (or, at least, assimilated in amounts too small t o affect the issue) has not yet been obtained. Moreover, there is the further question of whether both inorganic and organic substances unassimilated by zooplankton may be released from the gut in soluble form and not only as faecal material (Harvey et al., 1935; Harris 1959: see p. 154). Nevertheless, in the course of further experiments (Conover, 1966a) in which the nature and number of faecal pellets produced were such as to allow quantitative collection t o be made, direct measurements of assimilation were possible and gave results that compared closely with those obtained by the “ ratio ” method. All detailed studies of assimilation efficiency have so far been concerned with bulk constituents of the diet (carbon, nitrogen, phosphorus), not specific dietary fractions (sugars, proteins, fats). However, Cowey and Corner (1966),in the course of an investigation of the amino acids in various algal diets and the faecal pellets produced by C. finmarchicus when feeding on them, noted that amino acids accounted for a higher percentage of the dry weight of the faecal pellets when the animal fed on a high concentration of Skeletonem (s162 pg N/1) than when it fed on a low (E 14.2 pg N/l). These results indicated that the extent of assimilation of amino acids (protein) was related to the concentration of food available. The quantity of test material was so amall, however, that repeated amino acid analyses essential for an adequate statistical treatment of the data could not be made: the question therefore needs more detailed study. Nevertheless, these observations suggest that conclusions based on assimilation efficiencies measured in terms of a bulk constituent of the diet, such as nitrogen, may not necessarily apply in the case of a particular fraction of the diet, such as amino acids. So far, we have dealt only with measurements of assimilation efficiency made in laboratory experiments. I n contrast, certain studies carried out in the field have led to the conclusion that when plant food is plentiful the percentage of ingested material assimilated by ZOOplankton is by no means as high as that found in the laboratory. This phenomenon of so-called “superfluous feeding ” in the sea will now be considered.

E. Superfluous feeding Beklemishev (1962) holds that superfluous feeding occurs because animals stop increasing the quantity of food they assimilate when


137

the amount of plant food in the sea rises above a certain level. He observed that in various studies on the feeding of zooplankton a certain threshold level of algal food was reached beyond which neither growth nor reproduction was limited by the amount of food available. He calculated that this threshold value lay between 3 and 20 g biomass/m3, and proposed that superfluous feeding took place in the sea when the phytoplankton population rose above the lesscr of the two values, recalculated as corresponding to 390 mg C/m3 or 107-109 cells/m3. From an examination of phytoplankton data in various sea areas he concluded that superfluous feeding should be of widespread occurrence during one or two months in the spring. Among the consequences of this would be ( 1 ) a greater nutritive value of faecal pellets and (2) an increased rate of nutrient regeneration. Evidence of heightened nutrient excretion at a time when food is plentiful has been found in seasonal surveys of nitrogen excretion by Calanus hyperboreus in the Gulf of Maine (Conover and Corner, 1968) and of nitrogen and phosphorus excretion by C.$nmarchicus in the Clyde sea-area (Butler et al., 1969, 1970). However, Beklemishev’s view that assimilation is poor at times of year when plant food is abundant is based on the field observations of Harvey et al. (1935) for the English Channel and of Riley (1946, 1947) for Gcorges Bank off Cape Cod. A valuable and stimulating reappraisal of these-and other-field measurements of secondary production has recently been published by Mullin (1969) : accordingly, we need deal with them only in outline. The collecting of field data concerned with the production of ZOOplankton in the sea poses several problems. One is that the nets used to capture the animals may not provide a truly representative sample, larger members of the zooplankton tending to avoid capture and smaller members passing through the nets. Another difficulty is that factors other than grazing by the animals may reduce the plant population, part of which may sink out of the cuphotic zone or become dispersed over a wide area by water moverncnts. For these and other reasons Harvcy et al. (1935) and Riley (1947) emphasized the speculative nature of their conclusions. Briefly, Harvey et al. estimated the total production of phytoplankton during spring at Station L4 (English Channel) from the decrease in the phosphate content of the sea water. This fell by 7 mg P/m3 over a period of 60 days, giving an average daily production of phytoplankton phosphorus of 0.11 mg. The zooplankton present on any one day during the same period (mid-February to mid-April) contained an average of 0.29 mg P, roughly two and a half times that of the average daily plant production. Harvey et al. could find no

138

E. D.

S. CORNER AND ANTHONY 0 . DAVIES

evidence of diatom sinkage and concluded that all the plant crop had been grazed by the zooplankton. Accordingly, some 40% of the herbivores own weight was on average eaten daily. Harvey el a1. concluded that this was a maximal estimate: but as the animals probably returned phosphate to the sea as a soluble excretion product (see p. 152) the value for total plant production based on changes in the phosphate level in the sea could well have been an underestimate. Thus, the above value of 40%, as deduced from these data, was probably minimal. The green appearance of the faecal pellets produced by thc animals and the fact that the number of faecal pellets was closely related to the level of the phytoplankton population led to the conclusion that the quantity of cells eaten depended on the amount of food available instead of the dietary needs of the animals. Such needs wcrc lat8ercalculated by Harvey (1950) from data showing that 4% of the body weight was respired daily, and that 7-10% of the body weight was added daily as growth. These calculations, apparently based on values found with C. jinmarchicus and a mixed community of crustacean plankton, therefore indicated that 11-14% of the body weight was needed daily to replace respiratory losses and ensure growth. Thus, the finding by Harvey et al. that zooplankton grazed 40% of their body weight as plant food daily, and the further calculation by Harvey that only 11-14% was needed by the animals, led Beklemishev (1962) t o propose that about two-thirds of the captured food was unassimilated. Suporting evidence for this view was provided by the field observations of Riley (1946, 1947) in a study of zooplankton production on Georges Bank (Cape Cod, Mass.). From measurements of respiration rate, Marshall et al. (1935) had shown that the food requirements of C. $finmarchicus during winter were equivalent to 1.33.6% of the body carbon daily: in summer, the corresponding value was 1.7-7-6%. Riley (1946) used these data to show that a population of mixed zooplankton representing 1 g C/m2, would obtain its food requirements by capturing 0.75% of the phytoplankton (as g C/m2) daily. Riley (1947) therefore multiplied the daily values of the phytoplankton stock by a factor of 0.0075 in order to prepare a curve showing the consumption of the phytoplankton by the animals. This curve demonstrated that during the peak of the phytoplankton bloom (late April) the quantity of phytoplankton carbon consumed was nearly 30% of the body carbon in the animals. It was observed by Riley that the zooplankton assimilated nearly 8% of their body carbon daily during late March, the period when the rate of zooplankton growth reached a maximum. He concluded that this value of 8% represented the upper limit of digestion by the animals and that any food consumed in excess

PLANKTON I N NITROQEN AND PHOSPHORUS CYCLES

139

of this was unassimilated. Thus, at the peak of the diatom bloom the assimilation efficiency of the animals was only about 30%, a value close to that based on the calculations of Harvey et al. (1936) and Harvey (1950). This similarity is regarded as significant by Beklemishev (1962). Nevertheless, Riley made clear that his conclusions were to a large degree speculative, and more recent studies on the physiology and feeding behaviour of zooplankton indicate that several of his assumpThus, in Riley’s analysis all tions were-of necessity-oversimplified. the zooplankton were treated as herbivores, whereas it is now known that at least some of the animals present when the zooplankton reached its peak in mid-May (cyclopoids and Metridia spp.) could also have made use of animal diets. The use of respiration data obtained with a single species, Calanus jinmarchicus, in order t o calculate the body carbon used daily by a mixed population of zooplankton, is another obvious oversimplification, although admittedly the species was well represented (Riley and Bumpus, 1946). Moreover, there is now evidence that the respiration rate of Calanus jinmarchicus may be increased when the animals are actively feeding on high concentrations of plant food (Corner et al., 1965). In addition, Riley’s estimate of the daily food requirements of the animals does not seem to have included the quantity of captured food invested in growth, as well as that lost through respiration. Finally, basic in Riley’s analysis is the assumption that zooplankton organisms filter a constant volume of sea water irrespective of the amount of food material present : each animal eats a constant fraction of the phytoplankton population daily. However, recent studies with marine copepods have shown that filtering rates decrease with increasing food concentration, the amount of food ingested rising to a plateau and then falling (Mullin, 1963; Haq, 1967). The variation in filtering rate with food concentration has been discussed by Conover (1968) who, referring to the work of Ivlev with fish, points out that the rate of increase of the food consumed, d R , with an increase in the concentration of food available, dp, is proportional to the difference between the maximum ration, R,,,, and the actual ration, R. Thus:

dR --

dP

=k

(R,,, - R)or R,,,

= R (1

-e-kp).

Parsons et al. (1967), studying grazing by zooplankton, have modified this equation to :

R a9 .

= R,,, ( 1 - e k ( P 0 - p ) 1

there is a. minimum level of food, represented by p o , below which

140

E. D. S. CORNER AND ANTHONY Q. DAVIES

grazing will not start (approximately 70 pg C/1, Adanis and Steele, 1966; 50-190 pg C/1, Parsons et al., 1969). Clearly, some of the assumptions that have been made in order t o calculate assimilation efficiences from field data are to some extent oversimplifications. On the other hand, laboratory studies with zooplankton can also be criticized on the grounds t h a t thc animals are used under confined and unnatural conditions (although it is worth e~nphasizingthat findings made in the laboratory havc often been used at somc stage during calculations of secondary production in the sea). Accordingly, one may well expect to encounter differences between finduigs made in the laboratory and those made in the field. An example of such a difference is the finding by Conover (196Gb) that the average assimilation of Thalassiosira by Calanus hyperboreus feeding on a wide range of concentrations, including values wcll above that corresponding to 390 mg C/m3, was about 70% : whereas Beklemishcv (1962) regarded this level as the threshold at which superfluous feeding begins in nature, so that only about one third of the captured food should be assimilated. More recent studies, involving the use of both field and laboratory data, have shed further light on the question of superfluous feeding (Butler et al., 1970). The animal used was Calanus$nmarchicus and the calculations were based on measurements of nitrogen and phosphorus excretion as well as N : P ratios in the animals, phytoplankton and faecal pellets. It was found that even in a high concentration of natural phytoplankton, 77% of captured phosphorus and 62.5% of captured nitrogen was assimilated, values close to those observcd in laboratory experiments but much higher than those suggested by Beklemishev (1962).

IX. LEVELSOF NITROGEN AND PHOSPHORUS IN ZOOPLANKTON Recent measurements of the nitrogen content of zooplankton have employed the micro-Dumas method, using a Coleman Nitrogen Analyser (Butler et al., 1969, 1970; Herman and Beers, 1969). In earlier studies, however, both nitrogen and phosphorus contents of zooplankton have been determined after preliminary digestion of the samples with concentrated suphuric acid, the nitrogen then bcing estimated as ammonia after the normal micro-Kjeldahl procedure, and the phosphorus aa inorganic phosphate by the method of Murphy and Riley (1962). In some studies (e.g. Curl, 1962) there is reason to believe that digestion of the samples was incomplete and the data have not becn included in Table VI, which summarizes values found for both nitrogen and phosphorus, as percentage dry body weight, in various zooplankton from different sea areas.


141

The levels vary considerably, nitrogen ranging from 1.34% (Pleurobruchia pileus (0. F. Muller) to l l . l y o (Calanus finmarchicus) and phosphorus from 0.23% (Pleurobrachia pileus) to 1.70% (Balanus balanoides L.). On the other hand, nitrogen values obtained for certain groups of animals, such as copepods, are fairly similar, although the data apply to material collected from sea areas with different hydrographic and nutrient conditions. For example, Harris and Riley (1956) found that nitrogen accounted for 10.9yo and phosphorus 0.82% dry body weight of mixed zooplankton, mainly copepods, from Long Island Sound; and Beers (1966) obtained corresponding values of 12.2 and 0.79% respectively for copepods from the Sargasso Sea. The data of Beers (1966) confirm earlier observations by Curl (1962)in showing that nitrogen and phosphorus content varies with the wateriness ” of the animal. Thus, nitrogen accounts for 9-1 1 % dry weight in copepods and euphausiids-mysids (wet weight : dry weight ratio = 6-3-7.4 :I), 6 4 % in chaetognaths (wet weight : dry weight ratio = 14.7 : I ) and 1-4% in siphonophores (wet weight: dry weight ratio = 25 :I). Likewise, the phosphorus content of copepods is much higher that that of “ watery ” forms such as siphonophores and hydromedusae. Seasonal values for nitrogen and phosphorus were more constant for animals with lower water content. For example, in euphausiids-mysids, nitrogen varied from 9.43 to 10.46% dry body weight and phosphorus from 1.39 to 1.60% throughout the year ; but in ‘‘ watery ” forms, such as siphonophores, the range for nitrogen was 0-98-4-36% and that for phosphorus O-05-O~18~o. In the study by Beers (1966) the species composition and relative proportions of different stages of a particular group could have altered between monthly hauls, and this may account for the absence of any obvious seasonal trend in the levels of nitrogen and phosphorus. Evidence of seasonal changes is better sought using a particular stage of a single species, as was done by Orr (1934) with stage V Calanus jinmarchicus from the Clyde sea-area. Orr’s data, recalculated in terms of dry body weight, are presented in Table V I I and show that levels of nitrogen slowly increased from November to March. With the onset of the spring diatom increase, they then rose markedly to a maximum before falling throughout summer and winter to a minimum in October. Further evidence consistent with these findings is provided by Butler et al. (1969) who showed, using a mixture of Calanusfinmarchicus and Calanus helgolaizdicus from the Clyde sea-area, that females and stage V contained more nitrogen and phosphorus in spring than in autumn (see Tablc VI) ; also, Conover and Corner (1968) found that in Metridia (6

142

E. D. 9. CORNER AND ANTHONY (3. DAVIES

TABLEVI. LEVELS OB NITROQEN Specie4

swe

Sea Area

"

Copepods "

Mixed

North Sea

August

"

Sagitttas "

Mixed

North Sea

August

Nauplii Post-Larval Mature Mature Mixed

English Channel English Channel English Channel English Channel Long Island Sound Murman Sea

February June June June Jan-Nov

Norwegian Sea

June Average for year Average for year Average for year Average for year Average for year Average for year Average for year Average for year Spring Spring Spring Summer Summer Summer Spring Spring Autumn Autumn Autumn

~~

Time of Year

~

Balanua balanoidea Callionymw lyra (L.) Sagitfa elegam Verrill Pleurobrachia pileus " Copepods " Calanus finmarchicus Anomalocera patersoni Templeton Copepods Euphausiids-mysids Other crustacea Cheotognaths Polycheetes Siphonophores Hydromedusae Pteropods Cakmua finmarchicus Calanus helgolandicua

?

Adult Mixed Mixed Mixed Mixed Mixed Mixed Mixed Mixed Females Males V'S Females Males

v's

Mixed Calanua helgolandicus and Calanua finmarchicus Mixed small aopepods (mainly Pseudocalanus spp.)

Females V'S Females V'S Mainly IV and V

Sergasso Sea

Sargesso Sea s8rgaSSO Sea Sargasso Sea Sargesso Sea Sargesso Sea Sargasso See Sargesso Sea Clyde Clyde Clyde English Channel English Channel English Channel Clyde Clyde Clyde Clyde Clyde

?

Zonga (Lubbock) taken from the Gulf of Maine, nitrogen varied from

S - l l ~ odry body weight throughout the year, the maximum occurring in April and the minimum in September. The different chemical forms of the small quantities of phosphorus present in zooplankton have so far attracted little attention apart from the study by Sutcliffe (1965) of the ribonucleic acid contents of larvae of the mud snail Nassarius obsoletus Say and the brine shrimp, Artemia salina. By contrast, numerous studies have been made of the chemical composition of body nitrogen in zooplankton, most of which is present as amino acids, either in the free state or combined as peptides and proteins (see reviews by Corner and Cowey, 1964 ; 1968). High protein

PLANKTON IN NITROGEN AND PHOSPHORUS CYCLES A ND

143

PHOSPHORUS IN ZOOPLANKTON

N P N:P (% Dry wt) (% Dry wt) Weighl

Rdio Atoms

Referenem

10.35

1.58

6.52

14.4

Brandt and Reben

4.97

1.64

3.03

6.7

Brandt and Raben

9.70 8.24 9.24 1.34 8.91 10.2

1-70 1.60 0.95 0.23 0.82 1.07

5.71 5.16 9.78 5.81 10.9 9.53

12.6 11.4 21.7 12.8 22.9 21.1

Cooper (1939) Cooper (1939) Cooper (1939) Cooper (1939) Harris and Riley (1956) Vinogradov (1963)

11.6 9.62 9.96 7.83 7.84 8.92 2.97 2.89 3.25 11.1 8.9 9-6 10-7 9.1 8.0 11.1 7.6 9.1

0.82 0.79 1.48 1*26 0.63 0.99 0.14 0.17 0.30 1.16 0.99 0.80 1*20 1-17 0.91 1.16 0.80 0.75 0.55 0.61

14.1 12.2 6.74 6.23 12.4 9.01 21.2 17.0 10.8 9.6 9.0 9.5 8.9 7.8 8.7 9.55 9.45 12.1 10.9 12.8

31.1 26.9 14.9 13-8 27.6 19.9 46.5 37.5 23.9 21.2 19.9 21.0 19.7 17.3 19.2 21.1 20.9 26.7 24.0 28.3

Delff (1912) Beers (1966) Beers (1966) Beers (1966) Beers (1966) Beers (1966) Beers (1966) Beers (1966) Beers (1966) Butler el d. (1969) Butler el al. (1969) Butler el 01. (1969) Butler et d. (1969) Butler el d. (1969) Butler el al. (1969) Butler et d. (1969) Butler el d. (1969) Butler el al. (1969) Butler et al. (1969) Butler et al. (1069)

(1919)

(1919)

6.0 7.8

levels seem characteristic of many species. For example, Vinogradova (1960)gives values ranging from 55-61 % dry body weight for Euphausia superba Dana; Raymont et al. (1969), who determined protein dircctly by the biuret reaction, obtained values of 50-62% for Meganyctiphanes norvegim and 5 2 4 4 % for Thysanoessa inermis (Kr~yer);a value of 70% was found by Raymont et al. (1964, 1966) for Neomysis integer (Leach) and Leptomysis Zingvura (G. 0. Sars) ; Pavlova (1967) gives values ranging from 59.8-66.2% for various Black Sea cladocerans ; and Nakai (1955), estimating protein as body N x 6.25, obtained values ranging from 34-8-82-6% for several species of copepod from the Sea of Japan.

144

E. D. 9. CORNER AND ANTHONY Q. DAVIES

c.

TABLEVII. SEASONAL CHANQESIN NITROQEN CONTENTOF jinmarchicus FROM THE CLYDESEA-AREA. (Calculated from the data of om, 1934.) N

BS

yo body \vt

Month

5.91 6.40 6.95 7.11 7.41 9.80 9.80 8.00 8.00 7.65 6.95 6.80

Nov. Dec. Jan. Feb. Afar. Apr. May June July Aug. Sept. Oct.

Orr (1934),who also determined protein as body N x 6-25,found a reciprocal relationship between the levels of protein and lipid in Calanusfinmurchicus. The level of protein was maximal, 55%, in May when lipid was minimal, 22% : the protein level was minimal, 35%, in March when lipid was maximal, 45%. This inverse relationship has also beeen observed by Raymont et al. (1969) for Illeganyctiphanas norvegica; and for many other species by Nakai (1955),whose data show that although the levels of lipid and protein in the animals can vary greatly, the sum of both fractions remains markedly constant (82.0-89.5% dry body weight). Included in Table VI are various values for the ratio by weight of nitrogen to phosphorus. The ratio varies widely with different groups. For example, Beers (1966)found values of 6.23-6-74for euphausiidsmysids; 12.2-12.4 for copepods and chaetognaths; and 21.2 for siphonophores. Thus, the N : P ratio increases with the " wateriness '' of the animal. Redfield et al. (1963)proposed that the average ratio by atoms of N : P in zooplankton is 16.0 :1,fairly close to the value of 15.5 :1 for phytoplankton (see Section 111). However, Beers's data, when similarly expressed, show large departures from this value. Thus, his ratio for mixed copepods was 27.7:1, similar to an earlier high value of 24:l found by Harris and Riley (1956) but higher than that of 21.2:l calculated from the data of Butler et al. (1969). Beers also obtained a high value, 27.1 :1, for cliaetognaths: in fact, only his values for euphausiids-mysids and '' other crustacea " are near to that of 16.5:1 proposed by Redfield et al. (1963). Recently, Beers and Herman (1969)have determined the nitrogen and phosphorus contents of total, mixed zooplankton collccted from two hydrographic stations near Bermuda. Considerable variation was found during the two-year period of the survey. Thus, at one station, nitrogen varied from 0.77 to 14.5% dry weight (average 6.7%) ; and phosphorus from 0.06-1-1% (average 0.74%). At the other station, the range for nitrogen was 2.4-11% dry weight (average 7.5%); and the phosphorus range 0.25-1-2% (average 0434%). It is interesting to note that the average ratio of nitrogen to phosphorus by atoms waa


145

20.4:l at the first station and 20.0:l a t the other, both values being markedly higher than that of 16.0 :1 originally suggested by Fleming (1940).

X. NITROGEN AND PHOSPHORUS EXCRETION BY ZOOPLANKTON Curl ( 1962), discussing zooplankton production in Continental Shelf waters south of New York, wrote that The cotninunity metabolism of carbon only will be examined, inasmuch as the iieccssrwy data on nitrogen and phosphorus metabolism in marine anim& is almost totally non-existent.” I n recent years, numerous studies of this problem have been made, stimulated mainly by the relevance of nitrogen and phosphorus metabolism t o the vital question of nutrient regeneration (Ketchum, 1962), and the relation of nitrogen metabolism in particular to the important problem of protein synthesis (Gerking, 19G2 ; Cowey and Corner, 1963b). ((

A. Nitrogen excretion The first attempt t o measure nitrogen excretion by zooplankton seems t o have been that of Harris (1959) who estimated the quantities of ammonia excreted by catches of mixed zooplankton taken in Long Island Sound. The animals were placed in freshly collected sea water in the dark and the amount of ammonia excreted was determined as the difference between the levels present in the sea water a t the start and end of a 4-h period. I n most of Harris’s experiments the zooplankton consisted mainly of Acurtia clausi, and the results he obtained with these animals showed that they excreted on average 43.1 pg N/mg dry body weightlday. Earlier, Harris and Riley (1956) found that body nitrogen in zooplankton from Long Island Sound accounted on average for 8.91yoof the dry weight : accordingly, the animals studied by Harris (1959) excreted the equivalent of 48% of their body nitrogen daily. These tneasurements were made during spring (April 6-May 27) when a significant amount of particulate mate-ial was present in the unfiltered seawater and available t o the animals during the excretion experiments. As no allowance was made for the possible uptake of excretion products by this particulate material present as a food, Harris may have underestimated the total amount of ammonia excreted. A different approach t o the problem of nitrogen excretion was made by Cowey and Corner (1963b) who measured the average daily reduction in the levels of 16 amino acids in Galanus helgolandicus when the animal was starved over a period of 10 days. Measurements were made in both summer and winter, the daily fall in amino acids in the summer animals representing 2.1% of the total and the corresponding value

146


for winter animals 1.8%. The quantities of amino acids, both free and combined as peptides and proteins, in the related species Calanus jinmarchicus had earlier been estimated by Cowey and Corner (1 963a) as representing 11% of the wet weight of the animals. Therefore, assuming a wct weight : dry weight ratio of 6 :1, the starving Calanus lost 3.1% of their total amino acid content daily in summer, and 2.7% in winter. These values are an order of magnitude lower than those of Harris (1959) for Acartia, probably because the Calanus had been starved over a prolonged period. Corner et al. (1965) therefore measured nitrogen excretion by feeding Calanus, in a manner similar to that of Harris (1959), but with the added refinement that a correction factor was made for the small uptake of excreted ammonia by the plant food. Bacteria-free algal diets were used at various cell concentrations and it was found that nitrogen excretion increased with the food level. However, the increase was relatively small, a ten-fold rise in food concentration from 16 to 160 pg N/1. resulting only in an increase in nitrogen excretion from 9.3 to 12-2 pglmg dry weightlday (average values). The animals were therefore excreting approximately 8-1 1% of their body nitrogen daily, a level of excretion considerably higher than that found by Cowey and Corner (1963b)for Calanus starved over a long period, but still much lower than that found by Harris (1959) for Acartia. The average temperature used in the experiments with Acartia WM 13"C, compared with 10°C in those with Calanus. Corner et al. (1965) found that nitrogen excretion increased by a factor of 1.8 as the temperature was raised from 5 t o 15°C ; but the increase was too small to account for the difference between the excretion data for Calanus and those for Acartia. Harris used the method of Riley (1953) to estimate ammonia, but the procedure used by Corner et al. (1965) was an adaptation of the ninhydrin method described by Moore and Stein (1954). Ninhydrin reacts with nitrogenous substances other than ammonia (e.g. amino acids) but no significant difference was found between the levels of ammonia as determined by the ninhydrin procedure or Nesslerization (Barnes, 1959) or steam-distillation in a Kjeldahl apparatus. Corner et al. (1965) therefore concluded that significant quantities of nitrogenous substances other than ammonia were not excreted by Calanus. Moreover, had the plant cells been inefficiently captured and the contents " spilled ", or had they been incompletely digested, free amino acids contained in the algae could well have appeared in considerable quantities among the ninhydrin-positive substances present in the sea

147

PLANKTON IN NITROQEN AND PHOSPHORUS CYCLES

water occupied by the animals. Failure t o detect these substances in measureable amounts may therefore be taken to imply that neither of these processes occurred t o any notable extent. Johannes and Webb (1965) and Webb and Johannes (1967) found that considerable quantities of amino acids were released by mixed zooplankton collected in sea areas off Georgia and the Carolinas. These observations seemed inconsistent with the findings of Corner et al. (1965) and led Corner and Newell (1967) t o examine this question further, using Calanus helgolandicus. It was found by differential chemical analysis that these animals, whether fed or starved, excreted nitrogen mainly as ammonia, but that small and variable amounts of other nitrogcnous substances were also excreted. Corner and Newell (1967) concluded that one of these substances might be urea; and Jawed (1969) has recently found that small amounts of this substance are also excreted by Euphausia pacijim. Corner and Newell (1967) could not detect measureable quantities of amino acids, however, unless the test animals were used in unnaturally high density ; and they considered the use of very high concentrations of mixed zooplankton to be mainly responsible for the relatively high levels of amino acids observed in the studies made by Johannes and Webb (see Corner and Cowey, 1968). The experiments made by Corner and Newell (1967) have recently been criticized by Webb and Johannes (1969) who claim that bacteria attached t o the animals and their faecal pellets can remove amino acids (as well as ammonia) during excretion experiments carried out over long periods. Butler et al. (1969), in a study mainly concerned with nitrogen and phosphorus excretion by Calanus jinmarchicus at different seasons, examined the forms of nitrogen excreted over a short period by animals treated with a mixture of antibiotics and found that the amount excreted as ammonia still accounted for 78.3% of the total, a value close t o the average of 74.7% reported by Corner and Newell (1967). However, no estimations of amino acids as such were made and so the possibility remains that the animals may have excreted small quantities of these substances under bacteria-free conditions. Perhaps the true level of aminoacid excretion by zooplankton falls between the apparently high values found by Johannes and Webb (1965) (caused by overcrowding of the test animals) and the insignificant amounts found by Corner and Newell (1967) (because of bacterial contamination). Certainly the work of Jawed (1969), who has recently measured the rates of excretion of ammonia, amino acids and urea by Neomysis rayii Murdoch and Euphuusia pacijim would seem t o support this view. Thus, Jawed found that of the total nitrogen excreted by Neomysis rayii a t A.M.B.-O

6

148


lO"C, 76% was ammonia-nitrogen and 18% amino-nitrogen: for Euphuusia paciJica the values were 82% for ammonia-nitrogen, 13% for amino nitrogen and 1% for urea nitrogen. At lower temperatures the proportion excreted by both species as amino-nitrogen was significantly lower. Corner et al. (1965) concluded that the difference between Harris's (1959) excretion data for Acartia clausi and their own for Calanua Jinmarchicus was not related t o levels of available food, or different methods of chemical analysis, but probably reflected the fact that Acurtia is a very much smaller animal and therefore likely t o be much more active metabolically. Support for this view came from the finding that nitrogen excretion by the younger stages of Calanus Jinmurchicua (Copepodites 11, I11 and IV) was 21.6 pg/mg dry body weightlday compared with a value of 9.8 for adults. The dry body weight of the mixed young stages (24.6 pglanimal) was still considerably greater than that of the Acurtia clausi used by Harris ( 5 pglanimal). However, in a later study (Corner et al., 1967) data were obtained with nauplii and copepodites I and I1 (with an average dry weight of 5-5 pg) and B value of 38.1 pg N/mg dry body was obtained, reasonably close t o that of 43.1 found by Harris. I n addition t o food level, temperature and body-size as factors influencing nitrogen excretion, salinity may also have an effect. Thus, Raymont et al. (1968) have shown that Neomysis integer normally excretes 24 pg N/mg dry weightlday; but animals adapted t o full strength sea water and subsequently transferred t o 1% sea water show a temporary increase in excretion rate that can reach six times the normal value over the first two hours after transfer. The first attempt t o measure nitrogen excretion using a carnivorous species of zooplankton was that of Beers (1964) who found that the chaetognath Sagitta hispida Conant collected from St. George's Harbour, Bermuda, excreted ammonia a t an average rate of 12.7 pg/mg dry body weightiday, a value equivalent t o 14.5% of the total body nitrogen. No food was given t o the animals during the 24 h excretion experiment and so the value probably represents a '' basal '' rate of nitrogen excretion. Because changes in temperature and food level affect nitrogen excretion by Calanus it seemed likely that the animals might excrete different amounts a t different seasons. Seasonal variation was studied by Conover and Corner (1968), most of the data being obtained with the boreal-arctic species Calanus hyperboreus used in excretion experiments carried out a t P6OC. The animals were feeding during the experiments, either on natural particulate material or laboratory cultures of phyto-


149

plankton, and a correction was applied for the uptake of excreted nitrogen by the food. I n most instances this was neglible, and only in experiments involving Peridinium trochoideum (Stein) Lemm. as a food was it large enough t o invalidate the results. The average level of nitrogen excretion during spring (April-May) was 0.71 pg/mg dry body weightlday, compared with an autumn-winter (October-March) level of 0.30. Nitrogen on average accounted for 6.2% of the dry body weight and this value varied little with season. Accordingly, the animals excreted the equivalent of 1.1% of the body nitrogen daily in spring and 0.5% in autumn-winter. These values are much lower than those described for other species of zooplankton and probably reflect the large size of the animals (1-51 mg dry weight) and the low temperature of the experiments. A comparison was made between nitrogen excretion by fed and starved animals, and the pooled data from experiments carried out in spring and summer showed that the mean value for nitrogen excretion by animals fed on various food concentrations (ranging from 185-500 pg N/1) was 0.70 pg N/animal/day compared with a value of 0-58 for the starved. The additional quantities of nitrogen excreted by feeding animals in the experiments of Corner et al. (1965) and Conover and Corner (1968) are relevant to the point made by Harris (1959) that some of the ammonia released by zooplankton during feeding may not have been excreted as an end-product of metabolism, but released in soluble form with semi-digested faecal material. On the other hand, animals actively feeding may increase their metabolism above the “basal” level because of the additional work involved in digesting food. The release of ammonia-nitrogen with faecal material has not yet been demonstrated experimentally. However, evidence supporting the view that metabolic activity increases when the animals feed has been obtained from measurements of respiration rate. Thus, Corner et al. (1965) found that the rate of oxygen consumption by Calanus blgolandicus fed on Skeletonema was 86pl/mg dry body weightlday compared with a value of 38 for starving animals: significantly, rates of nitrogen excretion by the same batches of animals were in similar proportion, the feeding Catanus excreting 7.9 pg Nfmg dry body weightlday and the starving animals 3.6. Similarly, Conover and Corner (1968) found values of 21.5 and 16.6 pl.O,/animal/day for the respiration rates of feeding and starving Calanus hyperboreus, the corresponding values for nitrogen excretion being 0.70 and 0.58 pglanimallday : again, therefore, rates of oxygen consumption for fed and starved animals were in approximately the same ratio as the values found for nitrogen excretion.

150


TABLEVIII. LEVELS OF NITROGEN AND

Sea area

Species

Stase

Temp.

Season

Spring Spring Autumn Summer

Long Island Sound Narragansett BEY

Mainly Acartia clauai Mainly Acartia sp.

Adult Adult

13°C

Morrison's Pond (Nova Scotia)

Acarlia sp. Acartiu sp. Acarlia sp. Pseudocalanm minutua, Oithona similia and Temora longiwrnia Mixed Mixed Nwmysia integer

Nauplii CII-CIV cv-CVI Nauplii CoGpodites Adults

16-19'C Ii%19"C 16-19'C 16-19°C 16-19°C 16-19°C

Bras d'Or Lake (Nova Scotia) Gulf Stream Doboy Sound Test Estuary (English Channel) St. George's Harbour (Bermuda) Gulf of Maine Gulf of Maine

-

?

Summer

25°C

Summer

Adult

15°C

Summer

Sngitta hiepida

Adult

20oc

Calanus hyperborew Calanua hyperboreua

Adult Adult

4-6°C 4-6°C

Gulf of Maine Gulf of Maine English Channel

Calanua hyperboreua Calanua hyperboreua Calanua helgolandicua

Adult Adult Adult

4-6T 4-6°C 10°C

Clyde Sea-area Clyde Sea-area Clyde Sea-area Clyde Sea-area

Calanua jinmarchicus

0 0

10°C 10°C

Clyde Sea-area Clyde Sea-area Clyde Sea-area Sen Juan Island (Washington) Saanich Inlet (B. Columbia)

*

?

CII-CIV CI-CII & Nauplii

looc 10°C

Spring AutumnWinter Spring Spring Summer Winter Spring Spring Spring Spring

0

Spring Spring Autumn Summer

Neomyaia rayii

Adult

7°C 11°C 14°C 10°C

E u p h u a i a pacifica

Adult Adult

4°C 10°C

Summer Summer

Adult

4°C

Summer

$! and V $' and V

Percentage loss as amino acids ;

USW = unfiltered

808 wator ;

Oxygen consumption, unlike nitrogen excretion, is unaffected by the release of unassimilated soluble material from the gut and is a true measure of metabolic activity. The fact that nitrogen excretion increases to a similar extent when the animals feed is therefore consistent with the view that this, too, is essentially the result of increased

PLANKTON IN NITROOEN AND PHOSPHORUS CYCLES PHOSPHORUS

161

EXCRETED BY ZOOPLANKTON Nitrogen excreted daily

Food

A

/

llslmg

Phosphorus excreted daily \

Body wt

yo Body N

43.1 3.6 34

-

usw usw usw

-

usw

-

-

usw usw

-

-

24

-

FSW

12.7

14.2

48

-

-

/

Mlglmfl

Body wt 11 2.4 6-6 1.37 1.27 1.02 1.52 0.93 1.27 3.7 9.4

Reference

yo Body P Harris (1969) Martin (1968) Hargrave and Geen (1968) Hargrave and aeen (1968) Pomeroy et al. (1963) Raymont et al. (1968)

2.39

Beers (1964)

-

Conover and Corner (1968)

-

Cowey and Corner (19638)

-

Comer el al. (1966)

-

Corner el al. (1967)

-

Butler el d . (1970) Butler el al. (1969)

0.7 1 0.30

Algal diets Starved Starved Starved Algal diets FSW FSW FSW

0.70 0.58

9.3-12.2 9-8 24.6 38.1

FSW FSW FSW FSW

7.1 1-10.5 13.4 2-74 2.98

6.6-9.6 14.6 3.7 2.6

-

FSW FSW

1.73 2-47

1-6 2.1

-

FSW

1.44

1.2

-

-

\

-

usw usw

1.1

A

0.6

1-1 0.9 3*1* 2*7* 8-1 1 8.1 20 38

2.21 0.66

Jawed (1969)

-

~~~~~

FSW = filtered sea water.

metabolic activity and is not sensibly affected by the release of semidigested faecal material. Average values for rates of nitrogen excretion by zooplankton are included in Table VIII. The differences are considerable. However, a8 nitrogen excretion has been shown to vary with food level, tempera-

152

E. D. 5. CORNER AND ANTHONY 43. DAVIES

ture, salinity, season and body-size, and as only ammonia-nitrogen waa measured in some studies (e.g. Harris, 1959; Martin, 1968) but total nitrogen in others (e.g. Butler et al., 1969 ;Jawed, 1969), such differences are only to be expected. Generally speaking, the rates of nitrogen excretion by zooplankton are high compared with values obtained using other marine inverfebrates. For example, Dresel and Moyle (1950) give a value for amphipods of approximately 1.8 pg N/g dry weight/day; and Needham (1957) has shown that the crab Carcinides nu;cenas (Pennant), when fasting, excretes 44 pg N/g body weight/day. Small zooplankton of large surface : volume ratio occupying an aquatic habitat can probably dispose easily of the ammonia produced by protein breakdown ; and there are certain observations consistent with the view that some species make use of protein aa an energy source when starved (Cowey and Corner, 1963b ;Linford, 1965). Relevant to this are certain measurements of the atomic ratio (oxygen consumed : nitrogen excreted). Thus, the average chemical composition of particulate material in the sea (Redfield et al., 1963) is such that one atom of nitrogen should be excreted for 17 oxygen atoms respired. However, at a time when phytoplankton was scarce and zooplankton abundant in Long Island Sound, Harris (1959) obtained an 0 :N ratio of only 7.7, implying that protein was mainly being used as an energy source. Apart from evidence for the presence of “ peptidases ” in Calanus spp. (Manwell et al., 1967) and a-keto-glutarate transaminases in Neomy~is integer (Raymont el al., 1968) nothing is known about the various enzymes involved in the digestion and metabolism of nitrogen by the animals. Possibly this field of study will receive greater attention now that several species of zooplankton can be cultured in the laboratory.

B. Phosphorus excretion Cooper (1935) and Gardiner (1937) first showed that zooplankton rapidly increase the phosphorus content of sea water and Harris (1959) found striking evidence of this during his study of the nitrogen cycle in Long Island Sound. Thus, the data he obtained from experiments in which the zooplankton were mainly Acurtia clausi show that these animals excreted 11.0 pg P/mg dry weightlday. As Harris and Riley (1956) had previously found that phosphorus accounted for 0.82% of the dry weight, this excretion rate represented 130% of the body phosphorus daily. Harris’s excretion experiments were carried out over a short period (4 h) with animals used in natural sea water con-


153

taining particulate material as a food. However, Marshall and Orr (1 961), measuring phosphorus excretion by Calanus finmarchicus kept in membrane-filtered sea water for 6-24 h, obtained a much lower value. The animals had previously been fed on 32P-labelled unialgal cultures and it was found that equilibrium of 32Pthroughout the body was only reached after a feeding period of one week, after which the animals excreted a quantity of 32Prepresenting approximately 10% of the body phosphorus daily. Much higher rates of 32Pexcretion were observed, however, after the animals had fed for only 3 h on the labelled diet, presumably because 32Phad not reached equilibrium throughout the body. Conover (1961) concluded from these data that there must be a t least two “ pools ” of phosphorus in Calanus finmarchicus. One pool was labile with a half-life of only 0.375 days: the other pool was stable, with a half-life of 13 days. Calculating the relative sizes of the two pools, he showed that by far the greater fraction (94-99%) of the phosphorus was in the stable form, and concluded that the mean turnover rate for phosphorus through both pools was roughly 10% per day. Further experiments by Marshall and Orr (196l), howevec, showed that phosphorus excretion increased when the animals were feeding during the excretion experiments. Thus, the mean value obtained for phosphorus excretion in all experiments with starving animals-including those in which 32Phad not yet reached equilibrium-was ISYO, compared with a value of 25% for animals that had been fed. Studies on phosphorus excretion by mixed populations of ZOOplankton were made by Pomeroy et al. (1963) who measured changes in the levels of inorganic orthophosphate (estimated by the method of Hansen and Robinson, 1953) and total phosphorus (estimated by the method of Burton and Riley, 1956) in sea water containing animals from the Gulf Stream and Doboy Sound, Georgia. The experiments were made in summer a t 25°C and the amount of phosphorus excreted in the “ organic ” form was estimated as the difference between the levels of inorganic phosphate and total phosphorus excreted. It was found that about half the phosphorus excreted was in the “ organic ” form but the chemical composition of this fraction was not investigated. Samples of mixed zooplankton from the Gulf Stream excreted an average of 3.7 pg P/mg dry weightlday, of which 47% was “ organic ”, and samples from the estuarine Doboy Sound excreted 9.4 pg P/mg dry weightlday, of which 49% was “ organic ”. Hargrave and Geen (1968) made a detailed study of phosphorus excretion by Pseudocalanus minutus, Femora longicornis and Oithona similis Claus from Bras d’Or Lake and Acartia tonsa from Morrison’s

154


Pond (Nova Scotia) using the methods of Strickland and Parsons (1960) t o measure inorganic and total phosphorus. Phosphorus excretion was found to increase with temperature and salinity and to decrease when the animals were used at higher experimental densities. A further factor, influencing the excretion of inorganic phosphorus by Acartia tonsa, was time of day, excretion being maximal during the early evening when the feeding rate increases in the sea as Acartia migrate towards the surface. These animals were found to excrete about 40% more phosphorus when fed: an even greater increase was found in experiments with Pseudocalanus minutus and Oithona sirnilis. These various factors were used in predicting the quantities of inorganic phosphorus excreted by zooplankton under conditions prevailing in the sea. For the mixed species in Bras #Or Lake the predicted values, as pg P/mg dry weight/day, were 1.52 (nauplii), 0.93 (copepodites) and 1.27 (adults): those for Acartia in Morrison’s Pond were 1.37 (nauplii), 1.27 (CII-CIV) and 1-02(CV-CVI). The higher rate of phosphorus excretion observed with the younger stages of Acartia is similar to the finding described by Corner et al. (1965, 1967) for nitrogen excretion by the younger stages of Calanw. As in the study by Pomeroy et al. (1963) much of the total phosphorus excreted was ‘(organic ”, 74% being excreted in this form by Oithona, and 67% by Acartia and Pseudocalanus. However, in many of the excretion experiments plant food was present and the question arises whether all the phosphorus excreted by feeding animals represents true end-products of metabolism or includes soluble unassimilated material released with faecal pellets (Harvey et al., 1935). Relevant here are observations by Johannes (1964a) using the gammarid amphipod Lembos intermediw Schellenberg. He found that, compared with animals containing food in the guts, those with the guts empty released 75% less inorganic phosphate and 53% less ‘(organic ” phosphorus. However, as Johannes makes clear, food was superabundant in these experiments, the animals apparently eating at a rate too high for adequate digestion, and only 16% of the phosphorus captured was assimilated. This value is very much lower than that found by Marshall and Orr (1955a) and Berner (1962) for zooplanktonic animals, and it is worth noting that in a recent study the rate of phosphorus excretion by Calanus with food in the guts was compared with that of animals with the guts empty and no significant difference was found (Butler et al., 1970). It is also worth noting that studies on phosphate metabolism in certain mammals have shown that the excretion of body phosphorus can take place across the intestinal l i i g (see Wasserman, 1967).


155

Accordingly, even phosphorus released in soluble form from the gut of an animal may not necessarily represent material that has not been assimilated. Further light might be shed on this matter if determinations were made of both oxygen consumption (as an independent measure of metabolic rate) and phosphorus excretion by feeding and starving animals. So far, however, these experiments seem not to have been done. True, Satomi and Pomeroy (1965) have established a positive correlation between respiration rate and phosphorus excretion by zooplankton, but their findings do not include separate data for feeding and starving animals. According to Redfield et al. (1963) the complete oxidation of organic material with composition similarto that of plankton requires 276 atoms of oxygen per atom of phosphorus. Satomi and Pomeroy (1965) found an average value of only 72. One interpretation of this low value is that the estimations of excreted phosphorus probably included material that had not been amimilated (Corner and Cowey, 1968). Some recent evidence, however, supports the possibility, suggested by Satomi and Pomeroy (1965), that the animals excrete large quantities of phosphorus in an “ organic ” form which has not been completely oxidized. Thus, during short-term excretion experiments in which freshly-caught animals were given no food and the excreted phosphorus contained no undigested material, Butler et al. (1969) found that Calanus helgolandicus from the English Channel excreted small and variable amounts of “ organic ” phosphorus. These experiments were made in summer, however, and when identical experiments were carried out with CalanusJinmarchicus in the Clyde during the spring diatom flowering, “ organic ” phosphorus accounted for a much higher fraction of the total, the proportion varying (maximum 72%) with the amount of plant food that had been available to the animals in the sea immediately before the experiment (Butler et al., 1970). Phosphorus excretion by carnivorous zooplankton has so far received little study, the only data presently available being those of Beers (1964) for the excretion of inorganic phosphate by the chaetognath Sagitta hispida. These measurements, like those of ammonia excretion, were made with animals kept previously in the laboratory without food for 24 h and Beers regards the value found, 2-39 pg P/mg dry body weightlday, as a ‘‘ basal ” rate of phosphorus excretion. Even so, the value appears to be high in terms of total body phosphorus. Thus, Beers (1966) found that phosphorus accounted for 0.63% of the dry body weight of chaetognaths from the same sea area. It therefore seems probable that the Sagitta excreted some 40% of their body phosphorus daily.

156


C. Sea-sonul surveys of nitrogen and phosphorus excretion Data were obtained by Conover and Corner (1968) for nitrogen excretion by zooplankton at different times of year, but the first attempt to study both nitrogen and phosphorus excretion in relation to the seasonal production of phytoplankton was that of Martin (1968) using mixed zooplankton collected from Narragansett Bay. Martin found that the rate of nitrogen excretion (measured as ammonia by the Witting-Buch method : Barnes, 1959) by the animals was inversely related to the level of plant food available, the mean value in spring being 3.5 pg N/mg dry body weightlday (average plant population 17 x lo6 cells/l) whereas that in autumn was nearly ten times as high, namely 34 (average plant population 0.54 x lo6 cells/l). A similar trend was found in phosphorus excretion (measured as inorganic phosphate by the Deniges-Atkins method : Wattenberg, 1937), the mean spring level being 2.4 pg P/mg dry body weightlday compared with an average autumn value of 6.6. These data appear to conflict with the results of laboratory studies showing a positive correlation between nitrogen and phosphorus excretion on the one hand, and food level on the other. They also conflict with the observations of Butler et al. (1969) who, using Calanw Jinmarchicus collected from the Clyde, showed that the mean value for nitrogen excretion (measured as total nitrogen, both inorganic and organic, by the UV-irradiation method of Armstrong and Tibbitts, 1968) by females and stage Vs during spring was 13.4 pg N/mg dry body weightlday compared with an average autumn level of only 2.74 ; and that phosphate excretion (again measured as total phosphorus after UV-irradiation) averaged 2.21 pg P/mg dry body weightlday in spring compared with a mean value of 0.56 in autumn. In a further study (Butler et al., 1970), nitrogen and phosphorus excretion by Calanus in the Clyde was measured at all seasons, together with levels of the plant population as chlorophyll a. A summary of the data is shown in Fig. 6 from which it is clear that the levels of plant food and those of nitrogen and phosphorus excretion by the animals followed a similar pattern throughout the year. Corroborative evidence was provided by laboratory experiments in which animals fed on natural concentrations of phytoplankton at the time of the spring diatom flowering excreted more nitrogen and phosphorus than did starving controls. More detailed data from studies made during the early part of a spring diatom flowering are shown in Fig. 7. Although the peak levels of nitrogen and phosphorus excretion do not exactly coincide with

z a

- A

3

n

10-

4 10-

z

2 -e:

2 4

k

s O 6 - C

2

-

5

D.

5-

- x1 .

Y

01

- 55 -4

I FIQ.6. Nitrogen and phosphorus excretion as pgglmg dry body weight/day by Cdanua in the Clyde Sea-area between April 1968 and June 1969. 0 - 0. females; 0 - 0 , males; v - v , stage V. Stippled areas show chlorophyll a in 6 litres of BB8 water (E,B,B:) in a 10 ml acetone extract. (FromButler et d.,1970. Reproduced by kind permission of the Council of the Marine Biological Association of the United Kingdom.)

E. D. 9. CORNER AND ANTHONY a. DAVIES

158

,New generation o f 6 and V's

,Old generation of@, V'r LOld generation of

Q

I

Mixed Q

I First generatlon of Q

04

z1

-zm E

$02 Y al

2!

ti L

W

0

15 x

rrm -

.. E c

0

c)

f 5

Z

-.

W

05

FIG.7. Changes in nitrogen and phosphorus excretion (as pg/animal/day) by Calanus during the spring diatom increase in 1969. Symbols for animals and chlorophyll a as in Fig. 6. Hatched areas show diatom cell counts/litre. Horizontal scale expanded during April. (From Butler el al., 1970. Reproduced by kind permission of the Council of the Marine Biological Association of the United Kingdom.)

those of the plant food (in terms of cell counts and chlorophyll a ) there is clear evidence that a, dramatic increase in excretion rates follows closely upon the appearance of the diatom increase, and that excretion begins to fall once the initial peak of plant production is over.


159

The excretion experiments carried out by Butler et al. were begun as soon as possible after the animals had been taken from the sea and sorted in the laboratory. During this period the guts were emptied and, as no food was given to the animals during the four hour period of the experiments, the nitrogen and phosphorus excreted represented endproducts of metabolism and did not include unassimilated foodstuffs released in soluble form together with faecal material. The absence of food for this short period did not reduce excretion rates below those of feeding animals, Corner et al. (1965) having found that female Calanus actively feeding on Skeletonemu in the laboratory excreted 64-1 1.7 pg N/mg dry body weightlday, which compares closely with the range 7.11-10-50 obtained by Butler et al. (1970) with animals collected at a time when peak concentrations of diatoms, including Skeletonemu, were present in the Clyde. The question arises why the data of Martin (1968) conflict with those of Butler et al. (1969, 1970). Martin’s measurements of excretion rate were made with animals placed in unfiltered sea water containing natural phytoplankton, particulate material and microzooplankton. Thus, as the animals were feeding on diets normally available in the sea the excretion rates were more likely to represent those occurring in nature. However, no corrections were made for the possible uptake of excreted ammonia and phosphate by the phytoplankton, although the excretion experiments lasted 24 h. This uptake would have been greatest during spring when the food concentration was 17 x lo8 cells/l and nutrient levels in the sea were minimal (see Martin, 1965) and could have contributed to the low values found for nitrogen and phosphorus excretion at that time. The effect in autumn, however, when the plant population was only 0.54 x lo6 celIs/l and nutrient levels in the sea were higher, would have been much less, perhaps negligible. Another possibility is that whereas the species studied by Butler et al. was primarily herbivorous, the mixture of zooplankton used by Martin was dominated by Acartia tonsa during summer and autumn and this species can use both plant and animal diets (Anraku and Omori, 1963). Accordingly, the high levels of nitrogen and phosphorus excretion observed by Martin during the autumn could have been the result of animals feeding on microzooplankton. A summary of all the various data on nitrogen and phosphorus excretion by zooplankton is given in Table VIII and illustrates the very large degree of variation found. Such variation doubtless reflects the many different factors (e.g. food supply, body size, season) that can influence the final result. I n every case where both nitrogen and phosphorus excretion have been measured under the same conditions the

160

E. D. 8 . CORNER AND ANTHONY 0. DAVIES

quantity of phosphorus excreted is much less than that of nitrogen : yet, when excretion rates are expressed in terms of body phosphorus and body nitrogen, the proportion of body phosphorus lost daily is notably higher than that of body nitrogen. Generally, the turnover of both nitrogen and phosphorus by the animals is a rapid process, substantial quantities of dissolved nitrogen and phosphorus being returned to the sea water. Some ecological consequences of this are now considered.

D. Nutrient regeneration Several attempts have been made to assess the extent to which the excretion products of zooplankton supply nutrients required by the phytoplankton on which the animals feed. Thus, Harris (1959) computed the utilization of ammonia, nitrite and nitrate by plants in Long Island Sound as the amounts brought to the surface by vertical turbulence together with the small inorganic stock already present in the water. The sum of these quantities was 0.085 pg-atom N/1 at a mean depth of 7 m. The quantity of ammonia excreted by the animals was calculated from the average zooplankton population (about 0.1 1 mg dry weight/l) and the average excretion of ammonia (2.6 pg-atom N/mg dry weight/day) as 0-285 pg-atom N/1. The total amount of inorganic nitrogen consumed by the plants was therefore 0.370 pg-atom N/1, of which 77% was contributed by zooplankton. Balance sheets for nitrogen utilization and regeneration covering two further yearn were also provided by Harris who found that ammonia excreted by zooplankton accounted for 66% of the phytoplankton requirement in one and 43% in the other. The remainder was presumed to represent regeneration by bacteria and other organisms too small t o be captured quantitatively in the plankton nets. Martin (1968)) assuming a phytoplankton production rate of 10% daily, calculated that the Skeletonemu population in Narragansett Bay during spring required 1-89 pg-atom N/l/day. The regeneration of ammonia by the zooplankton was calculated as the product of the average excretion rate and the average biomass as 0.048 pg-atom N/1/ day, only 2.54% ofthe daily nitrogen requirement of the phytoplankton. On the other hand, during the autumn, when the phytoplankton population was much lower and nitrogen excretion by the animals much higher, the zooplankton were estimated to supply 181.7% of the daily needs of the phytoplankton. This excess ammonia apparently accumulated and contributed to the autumn maximum of nitrogen found in the sea. Martin applied similar methods in estimating the extent to which zooplankton excretion supplied the daily plant requirement for inor-


161

ganic phosphate. The value in spring was 16.9% and that in autumn 200%. Unlike nitrogen, excess phosphorus supplied by the animals in autumn did not accumulate in the sea. Geen (1965), using the 14Cmethod of measuring primary production, estimated the average summer rates in Bras d’Or Lake and Morrison’s Pond as 300 and 600 pg C/m3day respectively. From these data Hargrave and Geen (1968), assuming a C :P ratio for phytoplankton of 40 :1 by weight, calculated that 7.5 and 15 mg of inorganic phosphate were required daily to support photosynthesis by phytoplankton in these two sea areas. The total excretion of inorganic phosphate by the zooplankton population, estimated in the usual way, was 14.6 mg P/m2/day in the 20-m euphotic zone in Bras #Or Lake and 3.75 mg P/m2/day in the 3-m cuphotic zone in Morrison’s Pond. Thus, zooplankton supplied 195% of the daily phosphorus requirement of the phytoplankton in Bras d’Or Lake and 25% of that in Morrison’s Pond. These various estimates of the quantitative importance of the nitrogen excreted as ammonia, and phosphorus excreted as inorganic phosphate by zooplankton in supplying the nitrogen and phosphorus needed by the phytoplankton are complicated by the fact that: (a) some of the nitrogen and much of the phosphorus excreted by the animals may be present in an organic form and it is possible that these substances may also be used by the plants ; (b) microzooplankton may not be captured in the tow-nets, yet nutrient excretion by these small animals may be of considerable importance (Conover, 1961 ; Johannes, 1964b) ;and (c)nutrients excreted by benthic organisms may be brought into the euphotic zone by turbulence and further quantities excreted directly into the zone by fish. Nevertheless, in most of the sea areas studied nutrient regeneration by zooplankton appears to be of considerable, if not of primary importance in supplying the nitrogen and phosphorus requirements of the plants on which the animals feed. Moreover, Ketchum (1962) has drawn attention t o the contribution of migrating zooplankton to the vertical distribution of soluble nitrogen and phosphorus in the sea. Thus, some animals feed actively at the surface and later excrete these nutrients in the depths : others feed actively in the depths and later excrete nutrients near the surface. We have already mentioned that the average atomic ratio N : P in phytoplankton is about 16 :1 (Section 111), a value significantly lower than the average of 25 :1 found for zooplankton (Section IX).Ketchum (1962) has pointed out that zooplankton feeding on phytoplankton and retaining excess nitrogen in accordance with their tissue composition must show a relatively low N :P ratio in their soluble excretion products. Few data are available, but those obtained so far are consistent with

162


Ketchurn’s (1962) view. Thus, for the atomic ratio excreted nitrogen (as ammonia) : excreted phosphorus (as inorganic phosphatc) Harris (1959), using mixed zooplankton from Long Island Sound, obtained an average value of 9.7 ; and an average of 9.3 can be calculated from the data of Martin (1968) for Acartia spp. in Narragansett Bay ; furthermore, Beers (1964) obtained a value of 11-7 for the chaetognath Sagitta hispida collected off the coast of Bermuda. Butler et al. (1969) measured the ratio total excreted nitrogen (both inorganic and organic) : total excreted phosphorus (both inorganic and organic) for Calanus finmarchicus from the Clyde Sea-area and for Calanus helgolandicw from the English Channel and obtained an average value of 12.1. In a later study (Butler et al., 1970), using the same species, they found a small but significant difference between the N :P ratioin spring ( 11.0) and in winter (14.6). However, in general the N : P ratios for the soluble excretion products of zooplankton are fairly consistent, and lower than those found for either the animals or the plants on which they feed. Values for the N : P ratios in zooplankton, phytoplankton and the soluble excretion products of the animals have been used in calculations of feeding efficiencies ; and a more detailed treatment of this topic is given in the following section.

XI. GROWTH OF ZOOPLANKTON IN TERMS OF NITROGEN AND PHOSPHORUS An important quantitative aspect of the nitrogen (or phosphorus) cycle in the sea is the efficiency with which zooplankton convert dietary forms of this element into animal tissue. Of the food captured by zooplankton, only a fraction will be invested in growth or egg production, losses being incurred through incomplete assimilation as well aa through metabolic activities associated with maintenance. We have already seen (Section VIII) that the assimilation of nitrogen and phosphorus by zooplankton is, in general, a very efficient process : but also (Section X) that the metabolic losses represented by the levels of nitrogen and phosphorus excreted in soluble form by the animals are often considerable. In the present section we deal with various attempts to estimate nitrogen and phosphorus “ budgets ” for the animals, i.e. the proportions of captured nitrogen and phosphorus invested in growth and used in metabolism.

A. Rate of growth Growth rates of zooplankton, as daily increments in body nitrogen, have so far been obtained only with Calanusfinmarchicus (Corner et d.,


163

1967). A sigmoid growth curve was obtained for animals taken from the sea by combining data for the number of days between various stages, based on the field observations in the Clyde Sea-area by Nicholls (1933),with micro-Kjeldahl analyses of various naupliar and copepodite stages separated from tow-nets (see Fig. 8). A slow build-up of body nitrogen from egg (0.034 pg) to copepodite I (0.37 pg) occurred over a period of 13-5days, after which body nitrogen increased more rapidly to copepodite V (14.1 pg) over a further 11.5 days. From stage

Age (doys)

FIQ.8. Growth of Calanua jinmarchicw, in terms of body nitrogen. NI-VI, naupliar stages; CI-V, copepodite stages. (After Corner el al., 1967.)

V to adult female nitrogen increased by only 3.7 pg in a further 10.5 days. Thus, from egg to adult the animal laid down 17.8 pg N in 35 days, the sea temperature being 11°C. Mullin and Brooks (1970)found that rates of development of the related species Calanus helgolandicus were affected by temperature. Thus, the average time needed to grow from egg to adult female on a diet of Thalassiosira was 44 days at lO"C,compared with only 23 days at 15°C. Further evidence of faster growth at higher temperatures was found with Rhincalanus nasutus which, on the same diet, took 55 days to develop from egg to adult at lO"C,but only 36 days at 15OC. Faster

164


growth at higher temperatures was also observed by Heinle (1966) using Acartia tonsa cultured on the natural food available in the Patuxent Estuary. The time for development from " egg to egg '' waa found to be 13, 9 and 7 days at 15.5, 22.4 and 254°C respectively. Mullin and Brooks (1970) also showed that quality of diet affected growth rate. Thus, in experiments using Rhincalanus nasutus reared at 15"C, full growth was achieved in 23 days on a diet of Ditylum brightwellii, but required 36 days when the food was Thalassiosira jluviatilis. The field studies of Deevey (1960) have led to the generalization that copepods growing at low temperatures will be larger in size at any stage of development compared with animals of the same species growing at higher temperatures. However, Mullin and Brooks (1970) found no significant difference in carbon content between Calanw reared at 10 and 15OC on a diet of Thalassiosira ; and obtained a similar result with Rhincalanus nusutus reared on this diet. Further observations with the latter species also indicated that type of food had no sensible effect on size, inasmuch as animals reared on Dilylum or Thalassiosira did not significantly differ in carbon content. On the other hand, the quantity of food given does seem to affect size, for Paffenhiifer (1969) has found that the length of female Calanus helgolandicw feeding on the chain-forming diatom Lauderiu borealis ranges from 3-03 to 3-67 mm, depending on the level of food available. Possibly, now that a growing number of zooplanktonic species can be successfully cultured in the laboratory, the effects of temperature and the quality and quantity of food on the levels of nitrogen and phosphorus present in the animals can be studied. The exponential portion of the sigmoid growth curve (egg to copepodite V, Fig. 8) is represented by the equation W, = Woekt, where W, is the amount of any body constituent (carbon, nitrogen, etc.) after t days, W, is the quantity in the egg, t is the time increment and k is a rate coefficient (larger k values indicating more rapid development). In terms of body nitrogen, Corner et al. (1967) calculated a value of k of 0-24 for Calanus finmarchicus : but corresponding data for body phosphorus have not yet been obtained. Further data, described by Mullin and Brooks (1970) indicate that k values can vary considerably with temperature, type of food and stage of development. Thus, for Rhinealanus nasutus feeding on Thalassiosira at 10°C, Mullin and Brooks found k values of 0.13 (nauplius I to copepodite I), 0.15 (copepodite I to copepodite IV) and 0.06 (copepodite I V to adult). Corresponding valuee at 15OC were 0.15, 0.22 and 0.18 respectively. When Ditylum was used as a food the

PLANKTON IN NITROGEN AND PHOSPIIORUS CYCLES

165

k values for the later stages of growth were similar to those found in experiments with Thalassiosira : but during naupliar development the k value was markedly greater (0.64 compared with 0.15).

B. Egg production A further important aspect of zooplankton growth is the amount of nitrogen and phosphorus invested in egg production by adult femalcs. The number of eggs produced is known to be affected by factors such as the quantity and quality of food (Marshall and Orr, 1952 ; Edmondson et al., 1962) but so far the only estimate of the quantity of nitrogen involved in egg production is that of Corner et al. (1967) for Calanus finmarchicus, and no data have been obtained for egg production in terms of phosphorus. Earlier work by Marshall and Orr (1952) indicated that the average total of eggs produced by a female Calanusfinmarchicus was 250, over a period of 35 days: from which Corner et al. (1967) estimated the daily quantity of nitrogen involved t o be 0.25 pg (approximately 10% of the body nitrogen). However, Mullin and Brooks (1967) found a higher rate of egg production by the related species Calanus helgolandicus, mean values being 613 and 691 eggs per female over a period of 9 weeks. Even higher values have been found by Paffenhbfer (1969) using females feeding on phytoplankton cultures containing 25-400 pg particulate C/L, a range of concentrations similar to that found in ocean waters off La Jolla. The number of eggs Iaid was 1991 per female, a value close to that of 2 267 claimed for animals in “the wild ”. Paffenhbfer quotes no value for the nitrogen content of the eggs, but using the figure of 0.0345 pg N per egg found by Corner et al. (1967) for Calanus finmarchicus, about 70 pg nitrogen would have been released as eggs by each female. Assuming a dry weight of 250 pg, of which about 10% would be nitrogen, this means that roughly three times the nitrogen content of the female would have been used to form eggs. These figures therefore indicate that egg production by zooplankton is of considerable importance in the turnover of nitrogen (and presumably phosphorus) in the sea.

C. Net and gross growth eficiencies Two important factors in zooplankton growth are the fractions of captured food (K,) and assimilated food (K,) converted into new tissue, K , being defined as gross growth efficiency and K , as net growth efficiency (vide Conover, 1968). Values for these coeficients have been obtained for many species of marine zooplankton, but so far the data have been expressed only in

166


terms of a bulk constituent of the diet, carbon (Lasker, 1960) or nitrogen (Corner et al., 1967) for example, and no studies have been made with particular dietary fractions such as individual amino acids or lipids. Obviously, gross growth efficiency may be low in terms of a bulk constituent of the diet, such as phosphorus, which has a rapid rate of turnover (see Table 8), but could be relatively high in terms of particular phosphorus compounds. Qualitative considerations of zooplankton nutrition have been emphasized from another aspect by Harvey (1960) who pointed out that in order to obtain their maximum needs of a particular dietary constituent (e.g. an amino acid) the animals might have to capture, assimilate and metabolize an excess of others. The first attempt to calculate the growth efficiency of zooplankton in terms of nitrogen and phosphorus was that of Ketchum (1962), using the data of Harris and Riley (1956) and Harris (1959) for the ratios N : P in phytoplankton, herbivorous zooplankton and their excretion products. Harris and Riley (1956) found the average ratio N :P (in terms of weight N :weight P) for the phytoplankton in Long Island Sound to be 7.3 : I compared with a value of 10.9 :1 for zooplankton ; and Harris (1959) showed that the average value for this ratio in the soluble excretion products of the animals was 4-37:l. Ketchum gives no details of his calculations but presumably they were based on the following argument : over a finite period, food captured and assimilated by the animal is equivalent to the sum of the quantities invested in growth and expended in metabolism, i.e.

where R, and R, are the quantities of dietary nitrogen and phosphorus assimilated ; T, and T, are the quantities lost through metabolism ; WN and W, are the quantities laid down as new growth. RN Harris and Riley's (1956) value for phytoplankton gives = 7.3 RP WN and their value for zooplankton gives = 10.9. Harris's (1959) value W,

TN = 4.37. Expressing eqn (1) in terms of for excretion products gives phosphorus TP 7.3RP = 4.37Tp 10-9Wp (3) and as 7.3RP = 7.3T, 7.3Wp (from eqn (2))

+

+

T,(4-37 - 7-3) = W,(7-3 - 10.9) and T, = Wp

x

3-60 2-93'

__

(4)


167

Ketchum w u m e d that all the captured food was assimilated so that net and gross efficiencies are the same. Thus,

Ketchum concluded that this efficiency, nearly 50%, was excessively high. This is true for a value of gross growth efficiency (K,) but not of net growth efficiency ( K , ) (see Table IX). A further point is that the finite time considered by Ketchum apparently covered the whole period of growth of the animal, during which the N :P ratio of the diet and excretion products could have varied considerably. Similar calculations were made by Butler et al. (1969)to estimate net and gross growth efficiencies in terms of nitrogen and phosphorus for a mixture of Calanus helgolandicus and Calanw Jinmurchicus. In this case, however, allowance was made for the fact that some of the captured food was not assimilated, percentage assimilation of nitrogen being set equal to 62% and that of phosphorus 69% (average values taken from the literature). Butler et al. (1969)estimated the average value of K , for nitrogen as 33.1%, and for phosphorus 28*3%, these values being calculated as applying throughout the whole period of growth, but excluding egg production. Values for K , can also be deduced from the data, K , for nitrogen being 53.5% and for phosphorus 41%. A different method of determining feeding efficiencies, incorporating certain field data, was that of Corner et al. (1967)who estimated K , and K,,in terms of nitrogen only, for Calanus Jinmurchicus. Measurements were made of the quantities of nitrogen excreted and retained by the animals at individual stages of growth from egg to adult, using representatives of the various stages separated from tow-nettings. The times needed to develop from one stage to the next were taken from earlier field observations of Nicholls (1933). A value of 62% for percentage assimilation of nitrogen was incorporated in calculations of grossgrowthefficiency,giving 34% for K, with 55% for K,. Calculations were also made of K, for egg production, the number of eggs produced being taken as the average of 250 found by Marshall and Orr (1952). For egg production, K , in terms of nitrogen was 14% and K , 22.5%, values less than half those found for growth from egg to adult. As part of a seasonal survey, combining laboratory and field data, Butler et al. (1970)measured the increases in body nitrogen and phosphorus by a mixture of stage V, male and female Calanusjnmurchicus during a spring diatom increase in the Clyde. After nitrogen and phos-

168


TABLE Ix.GROSS( K , ) AND NET(Ks) Sea area

Basis for calculation

Calanua hyperboreua Calanua hyperboreua Calanua hyperboreua Calanua hyperboreua Acartia c l a w . Acartia clouai Acartia d a m * Acartia clam' Acartia clam' Acarticr Jawi Acarlia clauai Calunua helgolandicua Calanua helgolandicua Calanua helgolamlicua Calanua helgolandicua Calanua helgolandicua Calanua helgolandicua Cakcnua helgolandicua Calanua jinmarchicua Cakanua jinmarchicua Calanua finmarchicua Calanua finmarchicus Calanzu,jinmarchicua Calanua finmarchicua

Gulf of Maine Gulf of Maine Gulf of Maine Gulf of Maine Western Black Sea Western Black Sea Western Black Sea Western Black Sea Western Black Sea Western Black Sea Western Black Sea Western Black Sea Western Black Sea Western Black Sea Western Black Sea Western Black Sea Western Black Sea Western Black Sea Clyde sea-area Clyde sea-area Clyde sea-area Clyde sea-area Clyde sea-area Clyde sea-area

Dry weight Dry weight Calories Calories Calories Calories Calories Calories Calories Calories Calories Calories Calories Calories Calories Calories Calories Calories Nitrogen Nitrogen Nitrogen Nitrogen Phosphorus Nitrogen

Calanua finmarchicua

Clyde sea-area

Phosphorus

Penilia aviroattie Dana Penilia aviroatria Dana

Black Sea Black Sea

Dry Weight (orcalories)

Podon polyphemaidea Leuck. Evadne spinifera Miiller Euphauaia pacifia Sagitta elegana Cyanea capillata (L.)

Black Sea Black Sea N.E. Pacific B i s c a p e Bay S.E. Coast (Newfoundland)

Dry Weight (or calories) Carbon Dry weight Dry weight

Calculations do not include 16.670 lost as moults

phorus excretion by the animals had been determined in laboratory experiments the percentage assimilation of phosphorus, D,, wm calculated from the equation

PLANKTON I N NITROUEN AND PHOSPHORUS CYCLES

169

GROWTHEFFICIENCIES OF ZOOPLANKTON Stage of development

yo Aaaimilnletl K1 ~

CIV

cv CIV cv

Nauplii CI CII CIII CI v

cv

Egg product.ion Nauplii CI CII CIII CIV

cv

Egg production Growth t o adult Growth egg production Egg production Growth t o adult Growth to adult V's and adults (spring weight increase) V's and adults (spring weight increase) Young stages Growth + egg production by " average " female Growth egg production by " average " female Growth egg production Growth to adult Growth from 3-5 cm diameter

+

+ +

K,

food inetubolired

Reference

__

-

-

384

-

-

43

57

Conover ( 1964) Conover (1964) Conovcr (1964) Conover (1964) retipa (1967) Petipa (1967) Petipa (1967) Potipa (1967) Petipa (1967) Petipa (1967) Petipa (1967) Petipa (1967) Petipa (1967) Petipa (1967) Petipa (1967) Petipa (1967) Petipa (1967) Petipa (1967) Corner el al. (1967) Corner et al. (1967) Corner et al. (1987) Butler et al. (1969) Butler et al. (1969) Butler et al. (1970)

17.2

22.4

77.6

Butler et al. (1970)

40 40.3

54 54.5

46 45.5

Pavlova (1967) Pavlova (1967)

34.7 24.9 28.2 11.0 37

47.0 33.6 11.1'

53.0 66.4 72.3

Pavlova (1967) Pavlova (1967) Lasker (1966) Reeve (1968) Freser (1969)

3.7-13 13.e36.4 5-18 18-50 14 17

16 23 16 11 1 34 50 39 28 21 5 2 34 24 14 33.1 28.3 26.8

16.6 40.5 23.0 68.0 17 21 21 29 20 14 2.0 37 55 43 31 23 6 2.5

-

83.4 59.5 77.0 42.0 83 79 79 71 80 86 98 63 45 57 79 77 94 97.5

81.4

-

-

-

Where a, and a4 were the N :P ratios by weight in plant food and faecal pellets respectively, a3 was the N :P ratio for additional growth by the animals during this period, and rn was the ratio K,(N) :K,(P). As a percentage, D p was found t o be 77% and DN (percentage assimilation of nitrogen) was then calculated from the equation

170


As noted earlier (p. 140) these values, calculated at a period of the year when conditions in the Clyde Sea-area should have favoured “ superfluous feeding ”, are much higher than the poor levels of assimilation (22-33 %) used by Beklemishev (1962). Butler et al. (1970) made use of these data in preparing nitrogen and phosphorus “ budgets ” for spring growth by stage V, male and female Calanus Jinmurchicus in the Clyde. They found that of the total nitrogen captured each day. 26.8% was invested in growth, 37.5% was unassimilated and 35.7% was excreted in soluble form. Of captured phosphorus, 17.2% was invested in growth, 23.0% was unassimilated and 59.8% excreted in soluble form. The sum of the quantities of nitrogen or phosphorus used for growth, cxcreted in soluble form and voided as faecal material gave the daily ‘‘ ration ” required by the animals. This value, in terms of body nitrogen, was equivalent to 13.4% : that in terms of body phosphorus was 1 7 4 % . These values are similar to the range of 11-14yo calculated by Harvey (1950) in terms of body carbon (see p. 138). Values for K,(N) mid K,(P) were 42.7 and 22.3% respectively ; and for K,(N) and K,(P) 26.8 and 17.2% respectively. These K , values for growth by the more mature stages of the animals are lower than those calculated for the wholc period of development from egg to adult, and this observation is consistent with those of Petipa (1967) and Pavlova (1967) whose budgets for copepods in terms of calories show that both K, and K , values for growth by young stages are markedly higher than those for older animals (see Table IX). It is also interesting to note that the various data summarized in Table I X show that generally the growth efficiency of copepods in terms of egg production is lower than that calculated for growth from egg to adult : although a possible explanation of this may be that the total numbers of eggs produced have been undercstiniated (see p. 165). Values of K, and K, may be affected by factors other than stage of growth, one possibility being the level of availablc food. Thus, at times of year when food is plentiful the animal will have to expend additional energy in digesting and absorbing the large quantity of food it captures. On the othcr hand, when food is scarce the animal will have to work harder in order to capture its daily dict. This aspect of zooplankton nutrition has not yet been examined in terms of nitrogen and phosphorus, but evidence that K , diminishes at higher food concentrations has been found by Conover (1964) studying Calanus hyperboreus. Thus, the average K , value obtained at food levels greater than 6 mg dry weight/l was only 12-2%, compared with 25.3% at levels less than 3 mg dry weightll.


171

Mullin and Brooks (1967) have successfully reared Calanus helgohndicus and Rhinculanus nasutus in the laboratory and have now measured K , values under different experimental conditions (Mullin and Brooks, 1970). They found that neither temperature nor quality of food affected K,, and there was no regular decrease in K , with increasing age. The latter finding seems to conflict with those of Petipa (1967)and Pavlova (1967)but may be due to beliavioural differences between animals in the sea and those reared in the laboratory. Thus, Petipa (19G6)has drawn attention to the amount of energy used by animals in the sea when searching for food and when undergoing diurnal vertical migration. Using her earlier data (Petipa, 1964a ; l9G4b) she has calculated (Petipa, 1967) that the energy expended by older stages of Calanus helgolandicus migrating vertically over a distance of 50-100 m in the sea is 31-35 times as great as that of animals in the laboratory. By contrast, the smaller species Acartia clausi, which migrates over a much smaller distance (10-15 m), apparently maintains a constant level of metabolism. Petipa concludes that this is why K , values for the older stages of Calanus helgolandicus are lower than those for the older stages of Acartia clausi. Petipa’s claim that vertical migration can increase the metabolic rate of some zooplankton by as much as a factor of 35 seems difficult to reconcile with the view that migration between warm surface water and deeper cooler water provides an energy “ bonus ’’ for the animals (McLaren, 1963). It would be useful to know whether rates of excretion of nitrogen and phosphorus by animals vertically migrating are changed by this process sufficiently to affect K, and K, values, but so far this problem has not been studied. Relevant to our discussion of growth efficiencies is thc fact that values for K , have been used by Shushkina (1968)to calculate rates of production of various stages of a zooplankton population. From data in the literature relating respiration rate to body weight he calculated the oxygen consumption, T,and hence calories expended ; and from published values for K 2 , he estimated growth for each stage as

K2T . -

1 - K2 Combining these data with numbers and weights of animals in every stage of a population of Haloptilus longicornis (Claus)from the Fiji Sea, he calculated growth rate per day, P, as a fraction of biomass, B, for the various stages as 0.30 (copepodite 11), 0.06 (copepodite 111), 0.07 (copepodite IV), 0.03 (copepodite V) and 1.15 (egg production). There seems no reason why this procedure, described by Shushkina as “ t h e physiological method ”, should not be applied in calculations of rates of nitrogen and phosphorus production by a population of a particular

172


species of zooplankton in the sea, once excretion rates and K , values (or, preferably K 1 values, sincc these allow for the fact that not all the captured food is assimilated) for the species are known, and the neccssary field data are available.

XII. PLANKTON PRODUCTION AND NUTRIENT LEVELS CERTAINSEAAREAS In the previous sections we have been mainly concerned with laboratory studies of the uptake and release of nitrogen and phosphorus compounds by phytoplankton and zooplankton. In this final section we show how fluctuations in the sizes of plankton populations are related to overall changes in nutrient levels in certain sea areas and, in our discussion of partly enclosed regions, we deal with studies in which both physical and biological factors have been quantitatively assessed. IN

A. Temperate regions In temperate regions, nitrate and phosphate concentrations undergo marked seasonal cycles. During the autumn and winter the cooling of the sea surface and turbulence caused by stormsresult in the breakdown of the temperature stratification of the previous summer, and concentrations of nitrate and phosphate in the nutrient-depleted euphotic zone rise as mixing occurs with the deeper nutrient-rich water. I n the relatively shallow seas over continental shelf areas the whole of the water column may become homogeneous so that nutrient concentrations vary little with depth ; but in deeper water there is usually a marked rise in concentrations below the mixed layer. The increasing insolation of spring and early summer warms again the upper layers of the water promoting the formation of the thermocline ; and the combination of higher temperature, greater illumination and stability of the water column favours the multiplication of the phytoplankton. Rapid growth ensues and the nutrients are quickly diminished. The bloom is finally arrested when either one of the nutrients (usually nitrate) is depleted, or grazing by zooplankton limits the plant population. Some of the cells slowly sink below the euphotic zone where, in the absence of light, they cease to be viable and regeneration processes gradually return the nutrients contained in the organic matter to the water. Because of the thermocline, however, these reformed nutrients are largely prevented from being transported back into the euphotic zone and so remain unavailable until the following winter, although occasionally some vertical movement of the nutrients does occur to produce from time to time, resurgences of phytoplankton growth.

A

B

C

D

E

F

G

ti

J

0

I00

200

0

100

200

0

-u v)

01

E

100 .c_ v)

f a

8 200 0

f 00

0

100

A

B

C

D

E Stations

F

G

ti

J

200

Fio. $A. The seasonal variation of nitrate-nitrogen off the coast of New England. Concentrations an, in pg-atoms/litre. Stations A-G lay along 8 straight section stretching out, approximately perpendicularly to the coestline, across the continental shelf, and stations G-J were on a section parallel to the edge of the shelf. All stations lay within the region bounded by 39"-41"N 7lo-72OW. The vertical scale is expanded 400 times relative to that of the horizontal. (After Ketchum et al., 1958).

174

E. D . 5. CORNER AND ANTHONY a. DAVIES

The data of Ketchum et al. (1958) illustrate particularly well these seasonal changes in nutrient concentrations off the New England coast (Figs. 9A, B). In July 1957, the concentrations of nitrate-nitrogen in the upper 30 m were less than 1 pg-atom11 while inorganic phosphatephosphorus levels were 0-3-0-4 pg-atomll. We have already seen (Section 111) that phytoplankton tend to utilize nitrogen and phosphorus in the ratio 16 :1, so that here nitrate was the limiting nutrient. Below the euphotic zone, concentrations of both nutrients increaaed gradually with depth. By September, the phosphate in the upper layers was also depleted, indicating that, despite the almost complete absence of nitrate, phytoplankton growth had continued since July. The mixing of the water column, which had started in November, was complete by January so that from the surface to the depth of the continental shelf, nutrient concentrations were almost constant. Vaccaro (1963) found similar variations in the nitrate and phosphate levels in the same region, but also showed that, throughout the year, up t o 2 pg-atomsll of ammonium-nitrogen was present in the top 30 m, with occasional increases with depth. Vaccaro thought that thia ammonium-nitrogen provided an alternative nitrogen source enabling plant production to continue after the nitrate-nitrogen had been depleted. The origin of the ammonium-nitrogen was not investigated, but its excretion by zooplankton and presence in substantial quantities in rainwater (about 5 pg-atom NHt-N/l were found inrain collected in Bermuda by Menzel and Spaeth, 1962) were possible sources. The relationship between nitrite and nitrate concentrations in thia region has also been investigated (Vaccaro and Ryther, 1960). It was found that as nitrate-nitrogen increased to a level of 5.5 pg-atoms/l, nitrite-nitrogen increased in proportion in the ratio of 0.05 :l.Above this level, however, the ratio decreased. Concentrations of nitritenitrogen, which were always low, reached their highest values (about 0-3 pg-atomsll) in December. It was shown that the maxima innitritenitrogen concentrations, which were found just below the euphotic zone, might have been caused by phytoplankton releasing nitrite at low light energies. Planktonic organisms were also involved in the cycle of phosphom in the nearby Gulf of Maine, examined in detail by Ketchum and Corwin (1965). Concentrations of inorganic phosphate, particulate and dissolved organic phosphorus were measured on two occasions separated by ten days in April, 1964. A parachute drogue set at 10 m was used aa a marker for the surface water so that it would be possible to examine the same water mass at both times. Because of changes in the water column caused by movement of the water to a different location, the

175


variation of temperature and salinity with depth below 50 m altered during the intervening period and it was therefore necessary to compare changes in concentrations at isopycnal surfaces (i.e. where the water had the same density on the two occasions) for which salinity and A

E

C

D

E

F

C

H

July 1957

0

100

A

B

C

D

E

F

G

n

J

200

Stations

Fro. 9B. The seasonal variation of phosphate-phosphorusoff the coast of New England. Details aa for Fig. 9A. (After Ketahum el d.,1958.)

176


temperature readings were identical at both times. The vertical distribution of the three fractions of phosphorus, as well as the oxygen concentration, initially and 10 days later, are shown in Fig. 10. The inorganic phosphate in the upper 50 m decreased, there was no change at 50 m and then a slight increase down to the uT* value of 26-34 (average depth 113 m) below which it remained constant. The particulate phosphorus decreased slightly at the surface but there waa an overall increase for the upper 50 m due to the phytoplankton bloom in progress at the time: at greater depths, increases of particulate

1 1

0

0 2 5 050

0

Phosphorus (rg-atomll)

0.25

Oxygen (ml/l)

FIG.10. The distribution with depth of (A) inorganic phosphate-phosphorus;(B) particulate phosphorus; (C) dissolved organic phosphorus ;and (D)oxygen concentration, in water in the Gulf of Maine in April 1964. 0-0, initial values; 0-0 fins1 values. (After Ketchum and Corwin, 1965.)

phosphorus were caused by the sinking of moribund plant cells, but below the uT level of 26.54 (average depth 136 m) there was no change. The dissolved organic phosphorus increased in the upper 25 m, decreased below this and also remained constant below the uT level of 2645.

In the analysis of the data, the water column was treated aa a closed system. In the euphotic zone (depth 50 m), all the organic phosphorus was assumed to have been produced initially in particulate form, and derived from inorganic phosphate. Increases in particulate phosphorus below the euphotic zone were attributed t o sinking of the

*

uT = lo3 (e1 ) where e is the density of the water at temperature T referred to distilled water at 4°C.


177

phytoplankton ; and dissolved organic phosphorus was considered to be formed, at any depth, either by excretion or by the decomposition of particulate phosphorus. The phosphorus involved in the cycle : Inorganic P-t Particulate P+ Dissolved Organic P-t Inorganic P could then be calculated as (1) Decrease in phosphorus due to photosynthesis = Inorgaiiic P loss - Inorganic P gain Dissolvcd organic P loss = 14.20 - 2-72 4.99 = 1647 mg-atoms P/m2. (2)Organic phosphorus produced = Particulate P increase (euphotic zone below 50 m - Particulate P loss Dissolved organic P increase = (8.18 7.34)-0.60 1.43 = 16.35 mg-atoms P/m2.

+

+

+

+

+

+

The agreement between the two values was within the analytical error. The oxygen concentration in the upper 50 m increased by 41.8 l./m2, while below 50 m and down to the uT level of 26.34,there was a decrease of 14.6 l./m2. The increase in oxygen in the euphotic zone gave only a minimal estimate of photosynthetic oxygen production because on both occasions the water was saturated with the gas and there would have been a loss to the atmosphere. Ketchum and Corwin therefore used the method of Redfield (1948)to calculate from their data a value of the exchange coefficient of oxygen across the sea surface, and estimated that 9.7 l./m2 of oxygen were lost from the surface t o the atmosphere in the ten day period. Thus, the total oxygen production in the eupliotic zone would have been 51.5 l./m2. This value, in conjunction with thc phosphorus change of 16.47 mg-atoms/m2, leads to a A 0 :LIPratio of -279 :1. For deeper water, where the oxygen consumption corresponded to a decrease in dissolved organic phosphorus of 4-61mg-atoms/ m2, a ratio of -282 :1 was obtained. Both ratios are in good agreement with the geiicrally accepted value of -276:l (see Section 111). The dissolved organic phosphate (1.43 mg-atoms/m2)in the upper 25 m may have been excreted by zooplankton or released as extracellular products by the phytoplankton. However, as remineralization probably occurs independently of depth and there was a decrease of dissolved organic phosphorus between 25 m and 150 m of 4.99 mgatoms/m2 (average 0.04 mg-atoms/m3), it is likely that a further 1 mgatom/m2 of dissolved organic phosphorus was produced in the upper 25 m, increasing the total phosphorus cycled in the 10 day period to 17.40 mg-atoms/m2. mg-atoms P/m3/day The mean regeneration rate of 4.0 x meant that the rate of phosphorus assimilation by the plankton was

178

E. D. 9. CORNER AND ANTHONY Q. DAVJES

about eight times faster than its remineralization. Accordingly, Ketchum and Corwin suggested that the regeneration rate may be the factor which ultimately limits phytoplankton production. B. Tropical and sub-tropical regions In regions nearer to the equator, persistently higher light energies and temperatures allow phytoplankton production to proceed throughout the year and the regenerative processes are much more rapid. This causes faster cycling of thenutrients, and seasonal maxima and minima in their concentrations are therefore much less evident. For example, at a station off Bermuda in the sub-tropical northern Sargasso sea, Menzel and Ryther (1960) found that nitrate and phosphate levels remained low throughout the year (Fig. 11). In the euphotic zone (down to 100 m), nitrate plus nitrite-nitrogen varied from zero to 1.8 pg-atoms/l and phosphate-phosphorus between 0.02 and 0.16 pg-atoms/l. During the winter, when mixing of the water column down to the permanent thermocline at 400 m occurred, the nutrient levels at the surface reached their maximal values of only 1-2 pg-atoms N/1 and 0.1-0.2 pg-atoms P/I, indicating that only very low concentrations of regenerated nutrients were present in the waters below the seasonal thermocline. However, as in more temperate regions, use of the comparatively higher nutrient levels available in the euphotic zone in the winter was delayed until reformation of the thermocline prevented dispersion of the phytoplankton throughout the mixed layer. A shortlived bloom was then quicltly restricted by the exhaustion of the nutrients. Chlorophyll a levels (Fig. 11) showed that much of the resulting phytoplankton gradually sank below the euphotic zone and accumulated at 100-150 m where the nutrients regenerated from the plant material remained until the following winter. During the period of thermal stratification, when nutrient levels in the euphotic zone were very low, plant production still continued, probably because small amounts of nutrients were being supplied by vertical mixing with deeper waters and regeneration by zooplankton. The zooplankton population reached its maximal level at about the same time or just after the spring bloom (Fig. 11). During the remainder of the year their numbers were low and varied little. Menzel and Ryther (1961) thought that as the animal population was limited by the plant supply, any available phytoplankton were rapidly grazed and the nutrients regenerated, thus maintaining a " highly efficient biological system ". Menzel and Ryther (1960) found that there was no correlation between primary productivity in the ares and changes in nutrient

0

Nitrate t Nitrite-N (pq-otorns/L)

; ; 200 e,

el

E

I

400

f

600

800

0

Phosphate-P (pq-atomsI2)

200

'ji

r

L

4l

E 400

I

f

% 600 n 800 Chlorophyll o (mq/m3)

-pf f

e

0 20 40 60

n 80 100

1957

1

1958

I

1959

I-

8-

6-

4-

-

8

2-

-

O ' N ' D i J I F ' M ' A ' M ' J ' J ' A ' S ' 0' N ' D / J ' F ' M ' A

1957

1958

1959

WO.11. The seasonal variation of nutrients, chlorophyll a and zooplankton at station

s (32"N65"W) in

tho north-western Sargasso See. The zooplankton data were obtained by obliquo tows (with a 2 net) betweon 600 m and tho surface, and represent the dry weight of animal matter beneath 1 sq mjtre of surface. (After Menzel end Ryther, 1960, 1961.) AXE.-0

7

180


levels. During the first four months of 1958, for example, net carbon fixation within the upper 400 m amounted to 3.83 g-atoms C/ma. Assuming a carbon : nitrogen : phosphorus ratio of 100 :15 :1 in the resulting phytoplankton, this sbould have corresponded to a depletion of 0.57 g-atoms N/m2 and O.Oh8 g-atoms P/m2. In fact, in the same period, the nitrogen decreased by only 0.25 g-atoms/m2 and the phosphorus increased by 0.035 g-atoms/m2, indicating that regeneration of the nutrients was occurring at rates comparable t o or greater than their rates of assimilation during photosynthesis. It was pointed out, however, that the northern Sargasso Sea was not representative of the Sea as a whole: further south, the thermocline at 100-150 m was probably permanent so that phytoplankton production was always nutrient limited. Ammonium-nitrogen represents an important nitrogen source in this region also. Menzel and Spaeth (1962) found that in the euphotic zone concentrations of this form of the element were 2-4 times greater than the combined nitrite- and nitrate-nitrogen, and could be directly correlated with the amount of rainfall. Beers and Herman (1969) similarly showed that at stations close to the Bermuda islands, ammonium-nitrogen (which here also included labile amino-acid nitrogen) was more abundant than the anionic forms throughout the summer and early autumn, though nitrate concentrations rose very quickly at the start of the winter and soon reached their maximal levels. An interesting difference was found in the timing of the main phytoplankton bloom in these inshore waters of the Sargasso Sea as compared with the oceanic station used by Menzel and Ryther (1960). Beers and Herman (1969) discovered that phytoplankton levels-as measured by chlorophyll a concentrations-underwent a marked increase in late summer (Fig. 12). This was found t o be due to an increase in nutrients in the euphotic zone resulting from the breakdown of the thermocline at this time of the year (Fig. 12), though, here again, the outburst was short-lived and chlorophyll a levels soon returned to their normal values. The lateness of the plant bloom meant that the zooplankton population did not reach its maximum until the start of the following year (Fig. 12) (Herman and Beers, 1969). Excretion of phosphate by zooplankton may have contributed to the increase in concentration of this nutrient at night, for the animal population in the upper 200 m began t o increase in the afternoon and reached its maximal density at 21.00 h (Ryther et al., 1961). Ammonia levels in the euphotic zone seem at first glance to be unrelated to zooplankton excretion, for Beers and Kelly (1965) found that these

181

PLANKTON IN NITROOEN AND PHOSPHORUS CYCLES Nitrite + Nitrate Nitrogen

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levels decreased from a maximum in the morning (06.00-12.00 h) to a minimum near midnight. However, the low levels of ammonia found when zooplankton were at their peak may have resulted from the uptake of ammonia by phytoplankton during the night. In contrast to the northern Sargasso Sea, Ryther and Menzel(l965) found that stratification of the Arabian sea surface was permanent, and that nutrient levels increased quickly with depth so that high

182

E. D. S. CORNER AND ANTHONY G . DAVIES

concentrations were available just below the euphotic zone (50-100 m depth). In general, conccntrations were found t o be approximately twice those observed in the northern Sargasso Sea. The proximity of this supply of nutrients to the euphotic zone meant that any physical or meteorological process which caused turbulence would bring the nutrients into the surface waters and thus give rise to outbursts of high plant production. Such phenomena would probably account for the patchiness of phytoplankton production observed in this area. Also of importance t o the nitrogen budgets of tropical seas are the abundant colonies of the blue-green alga Trichodesmium found in these regions. The ability of these organisms t o fix nitrogen directly from the atmosphere was demonstrated by Dugdalc et al. (1964) though it is not yet certain whether the algae themselves, or associated organisms such as bacteria, are responsible for this. Trichodesmium is also able to assimilate ammonium- and nitrate-nitrogen (Goering et al., 1966) but, as the plant is normally present in waters which are low in nitrate, ammonium-nitrogen probably represents the chief supply of the element which is supplemented by direct nitrogen-fixation.

C . Polar regions The seasonal variation of nutrient levels in the Antarctic has yetto be described though plant populations (as measured by chlorophyll a) appear t o undergo normal seasonal cycles (El-Sayed, 1970), maximal levels occurring during the austral summer (Fig. 13). Although this region is usually considered t o be of generally high productivity, El-Sayed (1970) found that there was, in fact, a significant geographical variation, the waters nearer to the land ma.sses being considerably more fertile (by a factor of 5 ) than the oceanic waters. The surface waters in the Antarctic move northwards away from the continent and are replaced by the upwelling of deeper waters so that nutrient supplies in the area are continually being replenished. Nutrient levels, therefore, are rarely limiting, nitrate-nitrogen averaging 12.4 pg-atoms11 and phosphate-phosphorus 1-15 pg-atomsll. (El-Sayed, 1970). Concentrations are generally lower north of the Antarctic convergence where the northward moving waters sink below the surrounding sub-Antarctic waters ; but El-Sayed has pointed out that even there the levels of nutrients are generally higher than those corresponding t o the winter maxima of temperate regions. Nevertheless, the convergence does noticeably affect the productivity of the area, the phytoplankton standing crop t o the north of it being much smaller than that t o the south.

183

PLANKTON I N NITROGEN AND PHOSPHORUS CYCLES

In the Arctic the cover of snow and ice, which is present for a large part of the year, has a great effect upon biological activity in the sea. Apollonio (1958), working on an ice island, found that phytoplankton collected from beneath the ice showed signs of light-starvation. Lakes of melt water which form during the summer on the surface of the ice are believed t o act as lenses which concentrate the light and increase the plant production in the sea immediately below. The phytoplankton blooms which follow the receding edge of melting ice in the Arctic may similarly be caused by the higher level of radiation reaching the water in the absence of the ice. However, increases in nutrient levels may also play a part, as Grainger (1959) showed that at the time of the spring

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melt in the Canadian Arctic, the resulting decrease in salinity of the surface layers was accompanied by a considerable rise in the phosphate concentration (from 0-5 to 1.5 pg-atoms PO:--P/l) (Fig. 14) with smaller increases in deeper layers. This would seem t o indicate the presence of high phosphate levels in the ice, but no phosphate waa detected in the pack-ice (from a different location) which was analysed by Apollonio (1958). He did find, however, that nitrate levels in the ice (average 5.9 pg-atoms NO;-N/l) were significantly higher than those in the surface layers of the sea water below. In this connection, it is interesting to note that nitrate concentrations in the upper 50 m adjacent to the ice were always considerably lower (usually by a factor of at least 4) than those in the deeper water ; also that they decreased steadily throughout the winter from 2-3 pg-atoms NO;-N/1 in

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November to zero in May. The reason for this was not discussed but it may indicate a tendency for ice to accumulate the nutrient, which is returned to the water upon melting. Phosphate concentrations below the ice did not alter significantly during the same period, however, SO that, in this case at least, phosphate uptake by the ice did not occur. Bursa (1961), working at the same location as Grainger (1959), found that the phytoplankton bloom which began in May at the time of the spring melt reached its maximum in mid-August when phosphate levels had been reduced to their pre-melt values (Fig. 14). The bloom consisted very largely of the diatom Achnantes taeniata Grunow. By the end of September, the herbivorous zooplankton had almost completely removed the phytoplankton, and by late October, the ice cover had returned. A similar pattern of variation in the plant population (as measured by chlorophyll a ) was described by Apollonio for the water below the ice island, though the return of the snow cover at mid-August could also have helped to diminish the phytoplankton.

D. Partially enclosed sea area8 I n partially enclosed sea areas such as embayments or estuaries, nutrient levels often undergo cycles which are different, especially in timing, from those found in more open waters. I n Narragansett Bay, for example, nutrient concentrations are maximal during the summer months and are reduced to their minimal levels in the winter (Ferrara, 1953; Smayda, 1957; Pratt, 1965). Pratt (1965) made a detailed study of nutrient changes and plankton production during the period November 1959 to June 1963. The main phytoplankton flowering began in December or January and was followed by a succession of minor blooms which finished by early summer, the plant population consisting predominantly of Skeletonema costatum. While phosphate concentrations never fell below 0.3 pg-atoms PO;--P/l and were normally greater than this, nitrate concentrations became undetectable well before the peak of the phytoplankton bloom was reached, growth continuing for up to five weeks after nitrate had been depleted. The data obtained from a station at the mouth of the bay is illustrated in Fig. 15. I n the open sea, the stability of the water column is a necessary prerequisite to the inception of a phytoplankton bloom (Sverdrup, 1953); otherwise turbulence would cause the dispersal of the plant population. I n Narragansett Bay, however, the physical features are such that, in spite of tidal turbulence, the phytoplankton are effectively contained together (Smayda, 1957). Firstly, there is little interchange

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with the water outside the bay and only a weak surface current, SO that transfer of plant cells from the area is small ; secondly, the shallowness of the bay means that phytoplankton cells taken from the euphotic zone by water moving downwards are quickly returned t o it by complementary upward movements. Such a circulation of the plant cells extends the period of plant production, for only a fraction of the total population can photosynthesize a t any given time. Pratt (1965) pointed out that even before the main outburst of growth in the winter, the nutrient concentrations had, for several weeks, steadily decreased from the annual summer maximum although the phytoplankton population remained low during the same period. This was because of grazing of the growing plant material by the zooplankton which remained present in large numbers until the winter (Martin, 1965) : the temperatures then became too low for the dcvelopment of the principal zooplankton species in the bay (Acartia tonsa, Aeartia clausi and Oithona spp.) resulting in a reduction in grazing pressure which allowed the phytoplankton bloom t o proceed. Martin considered that grazing was, in fact, the main factor controlling the standing crop of phytoplankton throughout the year in this area, as the increasing zooplankton numbers consequent upon the rising temperatures of spring ended the plant outburst. The plant population was then gradually consumed and remained low from early summer until the following winter. Martin also suggested that the build up of nutrients which began in late summer was due t o their excretion by the zooplankton, the heavily grazed phytoplankton population being insufficient t o utilize the regenerated phosphate and ammonia. I n Long Island Sound, the seasonal cycles of the nutricnts are more like those found in open temperate sea areas, although here also, the inception of the main phytoplankton bloom is somewhat earlier (midJanuary t o the start of February) than usual. Riley and Conover (1956) studied the changes in nutrient levels and the concomitant variation in phytoplankton and zooplankton in the Sound over a period of two years (Spring 1952-Spring 1954): some of their data are illustrated in Fig. 16. Surface concentrations of phosphate-phosphorus varied from about 2.3 pg-atoms11 in the winter t o about 0.5 pg-atoms/l in the spring. Surface levels of nitrate-nitrogen were reduced t o almost zero by plant growth, and remained low until the end of the summer, after which they increased steadily back t o their winter maxima of between 15 and 20 pg-atomsll. There were slight increases in nutrient levels between the surface and the bottom during the first half of the year while, occasionally in the autumn, lower concentrations existed at the bottom than at the surface. Large rises in chlorophyll levels

188

E . D. S. CORNER AND ANTHONY 0 . DAVIES

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and cell numbers coincided with the decreases in the nutrient concentrations in late winter and several minor blooms took place up to the early autumn. Whereas the spring bloom was dominated by centrate diatoms, in the summer months dinoflagellates represented the bulk of the phytoplankton population (S.A. M. Conover, 1956), and the increase

PLANKTON

IN NITROGEN AND PHOSPHORUS OYOLES

189

in the zooplankton population which followed upon the spring outburst consisted largely of the copepods Acartia clausi and Acartia toma (Deevey, 1956). Water movement in the Sound has been shown to take place on two levels, nutrient-rich water flowing east to west into the bottom while the surface layers leave the area in the opposite direction (Riley, 1956a). In times of active plant growth, nutrients originally present in the surface layers are carried downwards in the organic material of sinking plant cells and the nutrient-depleted water moves away. The nutrients regenerated in the deeper waters are later carried back into the Sound. A nutrient conservation mechanism, analogous to that occurring in coastal upwelling situations, is thus in operation. Riley and Conover (1956) estimated that in 1953 this led to an average increase of 1-56 pg-atoms PO:--P/l and 0.96 pg-atoms NO;-N/l in the Sound. S. A. M. Conover (1956) confirmed, by enrichment experiments, that nitrogen depletion was the main factor limiting growth during the postfloweringperiod. After addition of nitrate to the water, growth occurred in test cultures to give normal population levels, but addition of phosphate caused only small increases in cell numbers. Harris (1959) investigated the nitrogen cycle in more detail and found that although nitrate was the main nitrogen source available during the spring outburst, the bloom was followed by considerable production of regenerated ammonia which, in the spring and summer, was present at concentrations at least as large as the combined nitrite and nitrate. A fall in the total nitrogen in the water from the original 19.5pg-atoms11 by mid-April was followed by a slight increase to 6 pg-atoms/l in June. These changes probably represented the sedimentation of particulate nitrogen to the bottom where, after some delay, nitrogen regeneration began to increase the level in the water. Harris also showed, using culture techniques, that ammonia was superior to nitrite and nitrate as a nitrogen source for the natural phytoplankton ; but, surprisingly, cell division did not occur in most of his experiments and the results were based on chlorophyll increases which were thought to indicate an improvement in the physiological condition of the plant cells. Riley (1956b), by assuming as a first approximation that horizontal diffusion and advection in Long Island Sound could be disregarded, has been able t o estimate the rate of change (R) of phosphate-phosphorus concentration caused by biological activity at various depths in the Sound throughout the year. The total rate of change of concentration at any point, on the basis of the above assumption, was set equal to the sum of the biological effects and vertical eddy diffusion, i.e.

190

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D.

9. CORNER AND ANTHONY 0 . DAVLES

where AP-, and AP, were the respective increments in phosphatephosphorus concentration between the mid-surface and the upper and lower surfaces of a layer of water of depth 22, changes being positive in a downward direction. The term in brackets represents the difference in rates at which the nutrient enters and leaves the layer due to eddy diffusion. Valuesof the vertical eddy diffusion coefficients (Az,A -*) were estimated from the temperature gradients in the water column, using a modification of the above equation t o describe the transfer of heat across each boundary. The value of R could then be calculated from the known rate of the phosphate concentration and the estimated rate of eddy diffusion. For the surface layer and that adjacent to the bottom, the above equation was adapted to allow for nutrient transfer across only one surface. An example of the calculation involved has been given by Riley : Period : 21 May-19 August, 1952, i.e. 90 days. Average depth of layer = 5 m. Increase in PO:--P : (1.00-0-51) = 0.49 pg-atoms/l. AP/At = 0.49/90 = 0.005 pg-atoms/l/day. Average increment in PO:--P, 0-5 m = 0.052 pg-atomsll. Average increment in POi--P, 5-10 m = 0.209 pg-atoms/l. Coefficient of eddy diffusivity, 0-5 m = 0.75 g cm-l sec-l. Coefficient of eddy diffusivity, 5-10 m = 0.68 g cm-l sec-'. Hence, rate of entry of PO;--P into layer from below = 0.048 pg-atoms/l/day and rate of loss of POi--P from layer to above = 0.013 pg-atoms/l/day. R = 0.005 - (0.048 - 0.013) = - 0-030 pg-atomsfllday which represents the average rate of phosphate-phosphorus utilization in the 2-5-7-5 m layer for the designated period. Similar caIculations were made for other depths in the water column covering observations made over a two year period. The results are shown in Fig. 17. Values of R for the early autumn were not estimated as eddy diffusion data could not be obtained for this period. The results show that in the 2-5 m surface layer, utilization of phosphate-phosphorus usually exceeded its regeneration to an extent that varied little throughout the year. At other depths, there were marked seasonal variations, maximal utilization occurring during the spring. Regeneration was greatest in the bottom layer adjacent to the mud surface during the summer

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months following the sedimentation of the phytoplankton. Vertical diffusion of the regenerated nutrient into the surface layer allowed phytoplankton production to continue so that, in the example quoted above, although the concentration of phosphate-phosphorus present at the start of the period would have been sufficient for only 17 days at the average rate of utilization, growth continued throughout the period and the nutrient concentration actually increased. Using a similar calculation, Harris (1959) was able to show that at a mean depth of 7 m in the spring of 1955, the net utilization rates of ammonium- and nitrite- plus nitrate-nitrogen were respectively 0.064, and 0.014 pg-atoms/l/day. However, these together represented only about 21 % of the total nitrogen assimilated during phytoplankton growth, the major part (77%) being supplied by zooplankton excretion (see Section X). Thus, although it involved only 15% of the total nitrogen originally present, the remainder having been carried to the

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192

E. D. 9. CORNER AND lLNTIiONY 0 . DAVIES

bottom in the organic material of the sinking plant cells, the phytoplankton-zooplankton-rcgeneratednutrient cycle waa the most important factor maintaining the turnover of nitrogen in Long Island Sound. Harris (1959) made the interesting observation that nutrient regeneration by zooplankton excretion is quite a rapid process and should quickly lead to equilibrium in the nutrient-plant-animal cycle as the nutrients are soon made available again for further phytoplankton growth. By contrast, bacterially-induced regeneration is a much slower process, von Brand et al. (1937) having shown in laboratory experiments that between 8 and 20 days were necessary for the release of 65-80% of the nitrogen in phytoplankton by bacteria. Moreover, Johannes (1968) considers that only a small proportion of nutrient regeneration is due directiy to bacteria : these organisms may, in fact, compete with plant cells for dissolved nutrients. These studies of partly enclosed sea areas have therefore emphasized the importance of zooplankton in the marine food web. For apart from providing a valuable source of food for higher trophic levels, these animals, by grazing and excretion, rapidly re-circulate nutrients that would otherwise be lost from the euphotic zone as sinking phytoplankton, thus ensuring that the period of primary production, on which relies the rest of the food web, is extended well beyond the phytoplankton bloom of early spring. XI11 ACKNOWLEDGEMENTS I n preparing this review we received much helpful advice from many of our colleagues, among whom we particularly wish to thank Dr G. T. Boalch, Dr J. H. Wickstead and Dr S. M. Marshall, F.R.S. We are also most grateful to Dr M. M. Mullin and Dr E. R. Brooks for kindly allowing us t o refer to work that had not been published. Our thanks are also due to the library staffs of the Plymouth Laboratory and the OceanographicMuseum, Monaco, for their patience and valuable help in obtaining numerous journals and translations of papers, particularly those in Russian ; t o Miss Brigitte Eisenhutt and Miss J. M. V. Irlam for typing the manuscript; and to Mr. G. A. W. Battin and Mrs. P. A. Ashton for re-drawing many of the figures. XIV REFERENCES Adams, J. A. and Steelo, J. H. (1966). Shipboard experiments on the feeding of Calanus jinmarchicua (Gunnerus). In ‘‘ Some Contemporary Studies in Marine Science ” (H. Barnes, ed.), pp. 19-35. George Allen and Unwin, London.

PLANKTON IN NITROGEN AND PHOSPHORUS CYOLES

193

Allen, M. B. (1963). Nitrogen fixing organisms in the sea. I n “ Symposium on Marine Microbiology ” (C. H. Oppenheimer, ed.), pp. 85-92. Charles C. Thomas, Springfield, Illinois, U.S.A. Anraku, M. and Omori, M. (1963). Preliminary survey of the relationship between tho feeding habit and the structure of the mouth parts of marine copepods. Limnol. Oceanogr. 8, 116-126. Antia, N. J., McAllister, C. D., Parsons, T. R., Stephens, K. and Strickland, J. D. H. (1963). Further measurements of primary production usingalargevolume plastic sphere. Limnol. Oceanogr. 8, 166-183. Apollonio, S. (1958). Hydrobiological Measurements on T3, 1957-58. (Unpublished manuscript). Armstrong, F. A. J. and Tibbitts, S. (1968). Photochemical combustionof organic matter in sea water, for nitrogen, phosphorus and carbon determination. J. mar. biol. Ass. U . K . 48, 143-152. Barnes, H. (1959). “Apparatus and Methodsof Oceanography.” Part I: Chemical. George Allen and Unwin Ltd, London. Baylor, E. R. and Sutcliffe, W. H. Jr. (1963). Dissolved organic matter in scawater as a source of particulate food. Limnol. Oceanogr. 8, 309-371. Beers, J. R. (1964). Ammonia and inorganic phosphorus excretion by the planktonic chaetognath, Sagitto hiapida Conant. J . Cons.perm. int. Explor. Mer, 29, 123-129. Boers, J. R. (1966). Studies on the chemical composition of the major zooplankton groups in the Sargeaso Sea off Bermuda. Limnol. Oceanogr. 11,520-528. Beers, J. R. and Herman, S. S. (1969). The ecology of inshore plankton populations in Bermuda. Part I. Seasonal variation in the hydrography and nutrient chemistry. Bull. mar. Sci. 19, 253-278. Beers, J. R. and Kelly, A. C. (1965). Short-term variation of ammonia in the Sargasso Sea off Bermuda. Deep-sea Ree. 12, 21-25. Boklemishev, C. W. (1962). Superfluous feeding of marine herbivorous zooplankton. Rapp. P A . R4un. Cons. perm. int. Expior. Mer, 153, 108-113. Benson, B. B. and Parker, P. D. M. (1961). Nitrogen/argon and nitrogen isotope ratios in aerobic sea water. Deep-sea Ree. 7 , 237-253. Berner, A. (1962). Feeding and respiration in the copepod Temora longieomia (Miiller). J . mar. biol. Ass. U.K. 42, 625-640. Brandt, K. and Raben, E. (1919). Zur Kenntnis der Chemischen Zusammensetzung des Planktons und einiger Bodenorganismen. W&s. Meeresunters., Abt. Kiel N . F . 19, 175-210. Broenkow, W. W. (1965). The distribution of nutrients in the Costa Rice Dome in the eastern tropioal Pacific Ocean. Limnol. Oceunogr. 10, 40-62. Bursa, A. S. (1961). The annual oceanographic cycle a t Igloolik in the Canadian Arctic. 11. The phytoplankton. J. Fiah. Ree. Bd Can. 18. 503-616. Burton, J. D. and Riley, J. P. (1956). Determination of soluble phosphate and total phosphorus in sea water and of total phosphorus in marine muds. Microchim. Acto, p. 1350. Butler. E. I., Corner, E. D. S. and Marshall, S. M. (1969). On the nutrition and metabolism of zooplankton. VI. Feeding efficiency of Calanua in terms of nitrogen and phosphorus. J. mar. biol. Am. U.K. 49, 977-1001. Butler, E. I., Corner, E. D. S. and Marshall, S. M. (1970). On the nutritionand metabolism of zooplankton. VII. Seasonal survey of nitrogen and phosphorus excretion by C&nw in the Clyde Sea-ha. J. mar. biol. Age. U.K. 50, 625-660.

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Adv. mar. Bwl., Vol. 9, 1971, pp. 205-2153.

TAURINE IN MARINE INVERTEBRATES J. A. ALLENand M. R. GARRETT Dove Marine Laboratory, University of Newcastle upon Tyne, Cullercacts, North Shields, Northumberland, England

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

I. Introduotion 11. Chemistry 111. Function IV. Summary and Conclusions V. Acknowledgements VI. Referenoes

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

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

.. . . . . . . . .

.. . . .. . . . .

205 215 227 240 241 241

I. INTRODUCTION Taurine, or 2-aminoethanesulphonic acid, while not usually considered as an amino acid is closely related t o them. It is listed in tables of amino acid content of invertebrate tissues (e.g. Simpson et al., 1959), sometimes with implied similarity of function, although this is by no means always clear. CH2.NH2 I TAURINE CH,.SO,H. Taurine was first discovered in the bile of the ox by Tiedemann and Gmelin (1827),and was thought at that time t o be an excretory product that was produced in the liver from the decomposition of a sulphurated acid contained in the bile and thus comparable chemically and physiologically with urea (Valenciennes and F r h y , 1855). Later work ehowed it to be widely distributed in the tissues of all the vertebrate groups (Kruckenberg, 1881a ; von Fiirth, 1903; Yoshimuda and Kanai, 1913; Berner, 1920; Walker, 1952; Awapara et al., 1950; Awapara, 1956; An and Fromageot, 1960; Basheri and Fromageot, 1962). Thus Awapara et al. (1950), found taurine in all the tissues of the rat that they analysed-liver, kidney, muscle, heart, spleen, testis, brain and ileum-and they found the greatest quantity in heart muscle. Muscles are said t o contain 75% of the body taurine of the rat, taurine constituting about 0.15% of the total body weight (Schram, 1960), but this figure, which is equivalent to 1200 p moles/lOO g tissue, may be an overestimate by at least two times (Boquet and Fromageot, 1965). 206

206

J. A. ALLEN AND M. R. GARRETT

TABLEI. THEOCCURRENCE OF TAURINE AND RELATED COMPOUNDS IN MARINE INVERTEBRATES (Taurine has been reported in all genera oxcept those marked with an asterisk).

Genw, Porifera Ficulina Haliehodria

Hymeniacidan Pachy m a t h a Thelia Geodia Calyx XeSl08pOngkZ

Cnidaria Actinia

Compound

Hypotaurine Hypotaurine Hypotaurine, Taurocyamine Hypotaurine Hypotaurine, Taurocyamine Taurobetaine Hypotaurine, Taurocyamine Monomethyltaurine, Dimethyltauhe

Anemonia Bunodea

Hypotaurine, Taurocyamine Hypotaurine Hypotaurine

Sagartia Anthopleura

Hypotaurine Taurocyamine

Metridium Corynactia Renilla Briareum Rhizoatoma Phyaalia Aurelia Polyzoa Chedoetornala Brachiopoda Terebratella Sipuncula Sipunculrla Phaacoloaoma

*Taurobetaine

Reference

Robin and Roche, 1954 Robin and Roche, 1954 ; Lange, 1965 Robin and Roche, 1954; Roche and Robin, 1954 Robin and Roche, 1954 Robin and Roche, 1954 ; Roche and Robin, 1954 Ackermann and List, 1959a and b Ackermann and Pant, 1961 Kittredge et al., 1962 Robin and Roche, 1954 Robin and Roche, 1954 Robin and Roche, 1954 ; Simpson et al., 1959 Robin and Rocho, 1954 Kittredge et al., 1962 ; Makisumi, 1961 Kittredge et d., 1962; Lange, 1965 Kittredge et al., 1962 Kittredge et al., 1962 Ciereszko et at., 1961 Haurowitz, 1922 Lano et al., 1966 Lane et al., 1966 Kittredge et al., 1962 Kittredge et al.,1962

*Taurocyamine *Taurocyamine, Hypotaurocyamine

Baldwin and Yudkin, 1950 Baldwin and Yudkin, 1950; Thoai et al., 1953a, 1963b ; Roche et al., 1962; Thoai and Robin, 1954; Robin and Thoai, 1962

207

TAURINE IN MARINE INVERTEBRATES

TABLEI (continued) BenurJ

Compound

Molluscs Patella Haliotie

Reference Ackermsnn and Janka, 1954 Konosu and Maeda, 1961 ; Kittredge et al.. 1962; Kurtz and Luck, 1935; Mendel, 1904; Schmidt and Watson, 1918 Krukenberg, 1881c Awapara, 1962; Simpson et d.,

Turbo Polinicea

1959

Crepidula Camidaria Hydrobia Littorina Septifer Olivia

Hypotaurine

Awapara, 1962 Krukenberg, 1881 Negus, 1968 Awapara, 1962 ; Kittrodge, 1962 ; Simpson el d..1959 Ouchi, 1959; Shibuya and Ouchi, 1957 Awapara, 1962 ; Simpson et al., 1959

Busycon

Tegula Faaciolaria

Awapars, 1962 ;Mendel, 1904 ; Mendel and Bradley, 1908 ; Simpson et d.,1959 Peterseri and Duerr, 1969 Awapara, 1962 ; Simpson et d., 1959

Murex

This

Awapara, 1962 ; Krukenberg, 1881c; Simpson et d.,1959 Awapara, 1962; Simpson et al., 1959

Siphonaria Bulk Doriopsis Arca Pectunculua Pinna Mytilua

Awapara, 1962 ; Bodford, 1969 ; Simpson et d.,1959 Kittredge et al., 1962 Krukenberg, 1881c Awapara, 1962 ; Krukenberg, 1881c; Simpson al., 1969 Krukenberg, 188 Krukenberg, 1 8 8 1 ~ ;Shibuya and Ouchi, 1957 Fraga and Lopez-Capont, 1959 ; Jansen, 1913 ; Lango, 1963 ; Potts, 1958; Robertson, 1965; Kelly, 1904 ; Yoneda, 1968 ; Bricteax-GrBgoire et al., 1964a; Karsten, 1845 ; Krukenberg, 1881c; Riegel, et al., 1949; Letellier, 1887 ; Allen and Awapara, 1960

%

208

J. A. ALLEN AND M. R. GARRETT

TABLEI (continued) Qenua

Reference

compound

MOllUSC8 Craeaoatrea Hypotaurine

Ostrm

Hillman 1966; Awapara, 1962; Simpson et al., 1959 Roe, 1965; Roe and Weston, 1965 ; Stasdeler and Frorichs, 1858; Suzuki, 1912; Valenciennes and FrBmy, 1855 ; Krukonberg, 1881c ; Tanaka, 1960

Bricteax-Gr6goire et al., 196413 Simpson et al., 1959 Drisko and Hochman, 1957 Kelly, 1904 ;Krukenberg, 1881c; Roe, 1965 Krukenberg, 1881c Okuda and Sanada, 1919 Simpson et al., 1959 Simpson et al., 1959 Potts, 1958 ;Simpson ed al.,

ctryphaeo Lithophaga Teredo

P&n Spondylue Avicula DonaZ Venue Doeinia

1959

Simpson et al., 1959 ; Allen and Awapara, 1960 ; Allen, 1961 Roe, 1965 ; Roe and Weston, 1965 ; Sugino et al., 1951 Simpson et al., 1959 Awapara, 1962 ; Simpson et al.,

Ran& Mactra Vo’olselb Noetia

1959

Brachwdontua Eledone

octopue

9

Sepia Desidicue

Isethionic Acid

Loligo

Isothionic Acid

Ommaetrephea

Simpson et al., 1959 Ackennann et al., 1923 ; Krukenborg, 1881a and b, 1882 Henze, 1904 ; Robertson, 1966 ; Fredoricq, 1878 ; Krukenberg, 1881b, 1882 ; Morizawa, 1927 ; Staedeler and Frorichs, 1858 ; Valoncionncs and FrBmy, 1855 Krukcnberg, 1881b, 1882; Lewis, 1952 Doffnor, 1961 ; Dcffnor and Haftcr, 1959, 1960; Kocchlin, 1954a and b. Koechlin, 1954a and b, 1955 ; Krukcnborg, 1882 ; Okuda. 1920; Deffner, 1961 ; Dcffner and Haftcr, 1959; Lowis, 1952 Kojima and Kusakabe, 1955; Suzuki et al., 1909

TAURIXE IN MdRINE INVERTEBRATES

209

TABLE I (continued) Benua Mollusca Loliguncula Annclida Arenicola

compound

Reference

Simpson el al., 1959 Hypotaurine, Taurocyamine, Hypotaurocyamine, Taurocyamine phosphate, Hypotaurocyamine phosphate

Nereia

Taurocyamine phosphate

Nerine

*Taurocyamine

Amphitrite

*Taurocyamino

Apomatua

*Taurocyamine, Taurocyamine phosphate *Taurocyamine phosphate *Taurocyamine, Taurocyamine phosphate *Taurocyamino, Taurocyamine phosphate *Taurocyamine phosphate Taurocyamine

Abbott and Awapara, 1960 ; Ackormann, 1955; Hobson and Rees, 1957 ; Thoai and Robin, 1954; Thoai et al., 1953a, b, 1963b ; Roche et d., 1960,1962 ; Baldwin and Yudkin, 1950; Ennor and Morrison, 1958 Kurtz and Luck, 1935; Hobson and Rees, 1955 ;Jeuniaux et al., 1961 Roche et d.,1960

phosphate

Neanthea Leichone Myxicola Glycera Sabelluria Serpula Clyrnene Protulu

*Taurocyamine, Taurocyamine phosphate *Taurocyamine *Taurocyamhe

Baldwin and Yudkin, 1950; Thoai and Robin, 1965 Thoai and Robin, 1965 Baldwin and Yudkin, 1950 Thoai and Robin, 1965 Roche et al., 1960; Hobson and Rees, 1955 Hobson and Rees, 1955 Kittrcdge et al., 1962 ; Roche et al., 1960; Thoai et al., 19538 Thoai and Robin, 1965 Roche et al., 1960 Robin et d.,1959; Roche el al., 1960

Pomatoceroe Adouinia Crustacca Calunua

Mitellu

*Taurocyamine, Taurocyamine phosphate Taurocyamine

Thoai and Robin, 1965 Kurtz and Luck, 1935 ; Robin etal., 1956 Webb and Johannos, 1967 ; Cowey and Corner, 1963 Kittredge et at., 1962

210

J. A. ALLEN AND M. R. OARRE'IT

TABLE I (continued) Gentia ~

Compound

Reference

~~

Crustacca Limnoria Ligicr Orchiatoidea Penaew Crangon

Drisko and Hochman ; 1957 Kittredge et al., 1962 Kittredge et al., 1962 Simpson et al.. 1959 Awapara, 1962; Fuchs, 1937 ; Roe, 1965 Kittredge et al., 1962 Jeuniaux et al., 1961 Suzuki et al., 1909; Kittrcdge et al., 1962 Okuda, 1920; Okuda and Sanada, 1919; Lewis, 1952 Bricteax-Grbgoire et al., 1962 ; Kermack et al., 1955 ; Dude1 et al., 1963 ; Porcellati, 1963 ; Florkin and Schoffeniels, 1985 ; Kravitz et al., 1963a and b ; Lewis, 1952 ; Stevens et al.,

Spirontocaria Palaemon Panulir iu, Palinzirua Homariu,

1961

Carcinzcs

Lewis, 1952; Duchlteau et al.,

lllaia Nept unua Pachygrapsua Cancer

Neopanope Pagurua

Lewis, 1952 Okuda and Sanada. 1919 Kittredge et al., 1962 Fraaer et al., 1952 ;Lewis, 1952 ; Stevens et al., 1961 Bricteax-Grbgoire et al., 19G2 ; Florkin et al., 1984 Awapare, 1962 Awapara, 1962 ; Simpson et al.,

Clibanariw

Awapara, 1962 ; Simpson et al.,

1959

Eriocheir

1959 1959

Limulua Echinodermata Thyone Slrongylocentrotus Arbacia Aster& Piaaater Aalropecten Luidia Tunicsta Cionu

Stevens et al., 1961

Asterubin

Simpson et al., 1959 Simpson et al., 1959 Holtfretcr et al., 1960 Ackermann, 1935 ; Jeuniaux, et al., 1962a, b Kittredge et al., 1962 Simpson el al.,1959 Ackermann and Janka, 1954 ; Kittredge et al., 1962

21 1

TAURINE IN MARINE INVERTEBRATES

Walker (1952) verified the results of Awapara et al. (1950), and found even larger amounts in the tissues of the cow. Taurine in conjugation with cholic a.cid in bile salts is commonly thought of as an cmulsifier of fat in vcrtebrates. Haslewood and Wootton (1950) and Jacobsen and Smith (1968) who tabulated all the information on bile salts to theso dates show that, with the Elasmobranchia as a possible exception, taurine is the conjugate in most vertebrate groups. However, it is now evident that it has other functions in addition t o this (Jacobsen and Smith 1968). That it is an end product of sulphur amino-acid metabolism is clear, but, its presence in quantity in muscle and nerve tissues suggests that it has other important functions. It was first found in invertebrates by Valenciennes and Frdmy (1855) who discovered it in abundance in the muscle of oysters and cuttlefish and then suggested that it probably had a much wider distribution than had been thought, a surmise that was t o be amply substantiated (Table I). Thus Kelly (1904) from estimations of the sulphur content of preserved and dried tissues of Pecten and Mytilus suggested that it constituted up t o 5 % of the dry weight (probably equivalent t o 120 p moles/kg and 1.6% wet weight). However, she assumed that all organic sulphur is in combination as taurine and an extraction from mascerated tissue could only get a yield of approximately 1% taurine. She explained the unexpected low yield by the difficulty of isolation. Subsequently it has been found in considerable quantities in other marine molluscs (Tables I1 and IV) (Mendel, 1904 ; TABLE11. MINIMUM AND MAxIrvrvnr CONCENTRATIONS or TAURINEREPORTED INVERTEBRATE PHYLA(Sources are the authoritics listcd in - Table I*)

IN THE MARINE

Phylum

Concentrations in p rnoleelg wet wt

Porifora Trace - 8 Cnidaria Present - 18 POly208 Present Brachiopoda Present Molluscs Present - 400 muscle 400, kidnoy 16, byssus 95, mantlo 73, blood 6, nerve 103t Annelid8 Prescnt - 3.6 Arthropoda Present - 90 muscle > 75, nerve 90, digestive gland 29, serum 0-6 p molct Echinodennata Present 39.2

-

*

t

For a detailed list of quantities in different generasee Jacobsen and Smith (1968). Maximum concentrations.

A.Y.B.-0

8

212

J. A. ALLEN A N D M. R. QARRETT

Henze, 1905, 1913 and 1914; Suzuki et al., 1909; Suzuki, 1913; Ackermann et al., 1924; Ackermann and Janka, 1954; Kittredge et al., 1962). Marine invertebrates other than molluscs have been found t o contain large amounts of taurine (Table I). It has been reported from the bryozoan Chilostoinata (Kittredge et al., 1962), the brachiopod Terebratella (Kittredge et al., 1962) and various polychaetcs (Kittrcdge et al., 1962; Kurtz and Luck, 1935; Duchateau et al., 1961), cchinoderms (Kossel and Edlbacher, 1915; Jeuniaux et al., 1962a and b ; Kittredge et al., 1962; Lange, 1964; Simpson et al., 1959), coelenterates (Lane et al., 1966; Kittredge et al., 1962; Simpson et al., 1959), crustaceans (Okuda, 1920; Kermack el al., 1955; Camien et al., 1951; Jeuniaux et al., 1961 ; Kittredgc et al., 1962; Simpson et al., 1959) and tunicates (Ackermann and Janka, 1954; Kittredgc et al.. 1962). Taurine has also been found in the cell wall of the bacterium Opaque and together with various methylated salts, in certain marine algae (Table 111). TABLE111. OCCURRENCE OF TAURINE AND TAURINE DERIVATIVES IN MARINEALGAE Genw,

Compound

Author

Polyaiphonia

Taurinc, D-CyStCillOliC acid

Ericson and Carlson, 1954 ;

Ceranium Chondrus

Taurine Taurinc, N(L-carboxyethyl) taurine

Porphyra

Taurine, Dimcthyltaurinc

Furcellaria Ptilotu Gelidium

Ericson and Carlson, 1954 Ericson and Carlson, 1954 ; Kuriyama, 1961 ; Young and Smith, 1958 Ericson and Carlson, 1954 ; Lindbcrg, 1955a Lindbcrg, 1955b Lindbcrg, 1955a Lindberg, 1955a

Dimcthyltaurino Taurinc, Dimethyltaurinc Taurinc, Monoxmthyltaurinc, Dimcthyl taurinc Taurine, N-(~-2,3-dihydroxy- Wickborg, 1956 n-propyl) taurino Kuriyama, 1961 N(L-carboxycthyl) tanrino Kuriyamn, 19til N(L-carboxyethyl) taurine Tagaki and Nnkamura, 1964 Taurino Ericsoxi and Carlson, 1954 ; Taririnc, D-cystoinolic acid Ito, 1963 Ito, 1963 D-cysteinolicacid Schwcigcr, 1967 Taurine

Gigartina Neodelsea Triilaea Deamareslia Ulva Enteromorpha Macrocystia

urukalle to Ras Hadd September As Sale18 to Ras a1 Hadd October Yarbat to a1 Khalat

FM A D J FYAMJ J S O N D J FMABIJ J A S 0 NDJ F M A-

700 800 700 700

50 300 300 220

35.103 240.103 210.103 144.103

(Distance to Cape Guardafui) 375 91.103 625 1 12.103 625 l12.103 375 94.103 375 94.103 200 61.103

720 720 920 1240 720 430

175 175 175 175 150 75

Defant (1936);Hart and Currie (1960); Berrit (1961, 1962); Darbyshire (1963); Buys (1959); Copenhagen 11953)

Swallow and Bruce (1966); Warren el al. (1966);Stommel and Wooster (1965); Foxton (1965)

126.103 Wooster el al. (1967); Ryther 1'26.103 et al. (1966);Lee (1963) 161.103 217.103 126.103 32.103

280

D. H. CUSHING

V. THE UPWELLING AREAS There are four types of upwelling area : (1) those in the main eastern boundary currents; (2) those in the Indian Ocean; (3) those in the equatorial system; (4) those in the domes. The World Atlas of Sea Surface Temperatures (U.S. Navy Hydrographic Office, 1944) gives charts by months, from which each upwelling area can be identified and its length and physical width determined ;the physical width was raised by a factor of 2.5 to give some indication of the biological width of the area, as described below. The seasonal distributions were worked out by months and the total area of the upwelling system was estimated. The areas of the more important upwelling systems are given by months in Table I11 ; in the column labelled seasons the peak months of upwelling are underlined. This method was adequate for the major upwelling system but, for the lesser ones, more specialist publications were consulted, as listed below. The column headed references includes papers which describe the particular system. I

45(

40

35

x

21

2(

I

I

I

II

Fm. 7. Mean temperatures off California at a depth of 10m for the years 1950-62 (Lynn, 1967); the hcavy brokcn line was drawn by eye where tho isotherms lie parallol to the coast,.

A. The width of the upwelling zone I n an earlier section, it was noted that the zone of biological production was probably wider than that of coastal upwelling. An attempt is made here t o make a better estimate of the width of the zone of production as a ratio of the width of the coastal upwelling. The 13-year mean temperatures at a depth of 10 m off California and Baja California, from 1950 t o 1962, are shown in Fig. 7 (Lynn, 1967). Because of the intense sampling in the area as part of the Calcofi programme, the distributions are well established. The physical boundary t o the coastal upwelling has been drawn by eye where the isotherms tend t o run parallel t o the coast. From Baja California t o Point Conception, the boundary is about 100 km offshore, but from Point Conception t o Cape Mendocino it may be nearer 200 km. Lynn has examined the same data in much more detail. All the temperature 130'

125'

......

.:

45.

-

400

-

35'

-

30'

-

120'

115'

I

I

I II

I

25'-

FIG.8. Distribution of correlation coefficients of tamperaturo on date at positions off California fitted to a harmonic regression (Lynn, 1967): the heavy broken line was drawn by eye using the coefficient of determination.

282

D. #. CUSHMQ

data were fitted, by Lynn, to a harmonic regression by date. The high correlat,ion of temperature with date shows the stable areas offshore, whereas upwelling is shown by low correlation coefficients. Figure 8 shows tlic distribution of correlation coefficients and tho line has been drawn by following the poor coefficients (using r < 0.75 as a criterion) at roughly 100 km offshore. Another way of showing the upwelling areas is given in Fig. 9, showing the months of occurrence of minima in temperature on the fitted regression curves and so the figure shows the

20°

FIG.9. Months of occurrence of the minimum of tho harmonic regression of temperature on dote off California (Lynn, 1967).

average position of upwelling by months. The areas are much closer to the biological boundaries and perhaps they indicate the direction of drift offshore from the coast. The width of the production zone can be examined in the zooplankton distributions off California from 1950-59 (Thrailkill, 1956, 1957, 1959, 1961 and 1963). A typical distriblltion is given in Fig. 10; the broken line is drawn at a median density. The width of the ZOO-

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UPWELLING AND THE PRODUCTION OF FISH

plankton zone was tabulated by year and area and averaged for the 10 years, ranging from 200-500 km. When the estimates from the temperature distributions are compared with those from the distributions of zooplankton, the ratio of width of productive zone to width of physical upwelling is 2.5. To treat all upwelling areas in the same way, the width is estimated from surface temperature distributions, and is raised by 2.5.

135"

130"

I

I

125"

120"

115"

I

I

110" I

L5" -

LO" -

3 0" cc of plankta

FIG.10. A typical distribution of zooplankton off California (Thrailkill, 1956); the broken line is drawn at a median density.

284

D. H. CUSHTNG

The biological width of the production zone is generated partly by the resultant of offshore and poleward transport and partly by the width of the productive zone generated by divergences upstream of the upwelling areas. The physical upwelling area tends to increme in width towards the equator. Then again some production is generated offshore of the dynamic boundary by the divergences associated with local wind stresses. Because the width of the area is of complex origin, its measurement is only empirical. B. Upwelling areas in the eastern boundary currents The four main upwelling areas are in the California Current, the Peru Current, the Canary Current and the Benguela Current. That in the California Current has already been described. The pattern of the poleward shift of upwelling during spring and summer as the high pressure areas move north and intensify is common to all four areas ; similarly, as the surface current moves towards the equator, a countercurrent moves poleward within the upwelling area in all four areas.

Peru Current I n the Peru Current, Gunther (1936) distinguished four regions of upwelling between Cape Carranza, south of Valparaiso, and the equator. The most northerly region lies between Punta Aguja in northernmost Peru and Santa Elena in Ecuador ; farther south is the region between Callao and the Guanape Islands just north of 10"s; the third region extends from Arica on the Chilean border t o Antofagasta about 300 miles south and the fourth to Cape Carranza. Here, the region has been divided a little differently to include the area south of Cape Carranza. Wyrtki (1966) distinguishes between the Peru Coastal Current-the region of coastal upwelling-and the Peru Oceanic Currents, the region of offshore divergences ; the first leaves the coast at about 5's and the second at about 10's and both currents stream westward into the South Equatorial Current. Between them flows the Countercurrent, mostly, but not always subsurface ; it is strongest at 100 m, but can reach 500 m. South of 15'5, upwelling comes from the lower layers of the Peru Coastal Current, but north of this latitude it is intense enough to draw water from the Countercurrent. Below the Peru Coastal current flows the Undercurrent, the analogue of countercurrents in other upwelling areas, the existence of which was confirmed by Wooster and Gilmartin (1961). Wooster and Reid (1963) have shown that the most intense upwelling probably occurs in this northern part of the area. Another characteristic of the Peru Current is " El Niiio ", which is a warm salty layer extending south over the Peru Current along the

UPWELLINQ AND THE PRODUCTION OF FISH

285

coast (Posner, 1957); it comes at Christmas time, which is why it is called El Niiio (the Little Boy), and is accompanied by northerly winds and heavy rain. It lasts until March and has occurred in particular years 1891, 1925, 1941, 1953, 1957-8, 1965-6 (Smith, 1969); as the period of heavy fishing in the anchoveta fishery starts at about this time, El Niiio is not welcomed because the fish are not accessible when it flows. The cause of the phenomenon is not known exactly, but Bjerknes (1961) has suggested that it is associated with changesin the atmospheric fluctuations which cause a transequatorial flow from the Equatorial Countercurrent. Thus there are two differences in the Peru Current from the common pattern, the more prominent countercurrent and the periodic occurrence of El Niiio. Canary Current

Until very recently, the Canary Current had not been very well described. The charts of surface temperature (U.S. Navy Hydrographic Office, 1944) summarize much of the early historical data. Furnestin (1959) examined the area between Cap Jubi, in the latitude of the Canary Islands, and north of Casablanca ; quarterly cruises and some sections show upwelling to some extent between Cap Ghir, just north of Agadir, and Mazagan, just south of Casablanca. A further upwelling appears late, north of Casablanca, and in late summer it occurs on the Iberian coast as far north as Vigo in north-western Spain. But the upwelling off Portugal has not been explicitly studied. Jones and Folkard (1968) have published sections of the whole current and show that upwelling is limited to the top 200 m, as in other areas. Surveys were made in March, June and October in the area ; that in March extended from Cap Blanc, halfway between Dakar and the Canary Islands and Cap Juby, that in June from the Gulf of Cintra, just south of Cap Blanc, to Cap Juby and that in October/November from Dakar to Cap Ghir. There is enough information t o show that there is a seasonal shift of upwelling to the north, and near Cap Blanc it is possible that the water rises from depths a little greater than 200 m and perhaps there is some evidence of a countercurrent. A remarkable point from their sections is the apparently slow rate of mixture of various properties and the upwelling tongue sometimes bends downwards t o seaward. The region between Freetown and Dakar has been examined by Berrit (1958, 1961, 1962), who has shown the shift with season from Cape Vergas in Guinea northwards as winter gives way to spring. It is in this region that the Canary Current turns westward into the North Equatorial Current ; south-eastwards, the Guinea Current and, to seaward, the Equatorial Countercurrent flows into the Gulf of Guinea. The latter will be

286

D. H. CUSIIINO

examined in a later section. The distinctive character of thc Canary Current region really lies in the shape of the coast, i.e. the entrance to the Mediterranean and the turii to the eastward of the coastline in the south ;in detail, the coast is rather indented with prominent capes, with upwelling taking place to the south of each.

Benguela Current In the Benguela Current, the upwelling area was described by Defant (1936) and Hart and Currie (1960) have published a thorough study of it. They showed a southward seasonal shift and demonstrated the presence of a countercurrent below about 200 m ;they also described the " roller bearing " of convergence and divergence about 100 km offshore which corresponds to Sverdrup's dynamic boundary. Buys (1959) and Darbyshire (1963) have published charts of surface temperature and have described the system of upwelling. Stander (1964) has studied the area north of the Orange River and concludes that the most frequent and intense upwelling occurs between the river and Luderitz about 200 miles north of the Orange River and that as far as Cape Cunene upwelling in the northern part of South-West Africa decreases northwards. Seasonally, upwelling starts off South-West Africa in midwinter and continues in the spring. Orren and Shannon (1967) point out that north of 30"s the upwelling season occurs in spring and early summer, whereas south of that latitude it takes place in summer and early autumn. Thus there is a poleward progression of the upwelling from early spring to early autumn as in other areas. Bang (1971) divides the upwelling zone into four sections outward from the shore, (1) an inshore region where the centres of upwelling are, (2) an intermediate zone with frequent thermal inversions, (3) an offshore divergence belt, (4) and lastly the oceanic trade-wind drift. There is a belt of slicks running from SSE to NNW 100 km offshore, which were observed on radar, as strips of calmness in the surface roughnesses. Jones (1968, 1971) has described the upwelling system in February 1966 ;he distinguishes between active and quiescent systems, the latter being characterized by high surface salinity inshore with low, not high, nutrient levels. So when upwelling stops, the algal production continues, taking up nutrients, perhaps without the grazing restraint (because I believe that the grazing actively restores nutrients to the water due to the destruction of algae). Figure 11 shows the surface temperature distribution for a 2-year period between Cap Frio, in South-West Africa and Cap Timiris, north of Dakar (Berrit, 1961, 1962). The cold water, indicating a seasonal coastal upwelling, is shown as stippled and shaded areas on the diagram. There is a seasonal alteration between the Canary Current in the north


287

Cap Timiris Dakar Cap Vergas Monrovia Cap des PalmesAbidjan Cap des 3 Pointes Lomd Cotonou Lagos Cap Formose Douala Bata Cap Lopez Pointe Noire Loanda Lobito Mossamedes Cap Frio Fro. 1 1 . The distribution of inshore temperatures between Cap Timiris, north of Dakar, and Cap Frio in South-West Africa. T h e position and timing of upwelling in the Guinea Current in relation to that in the Canary and Benguela Currents (Berrit, 1962).

and the Benguela Current in the south. From January to May there is upwelling from Cap Vergas, in Guinea, to north of Cap Timiris, which retreats to the north in the northern summer and returns in the late northern autumn; from May to October there is upwelling from southern Angola to beyond Pointe Noire, which retreats in the southern

288

D. 11. CUSHINO

summer-timc and returns in the late autumn. At the same time, Fig. 11 shows the shift of upwelling away from thc equator from spring to summer in both the two major West African upwellings. Between Cap des Palmcs and Cotonou, i.e. off the Ivory Coast and Ghana, there is another upwelling, which appears to be linked temporarily to the Benguela upwelling. But it is likely that it is associated with the WSW winds in summer in the Guinea Current, which is an extension of the Equatorial Countercurrent ; during the same season, the Guinea Dome is established south-west of Dakar as the countercurrent turns into the North Equatorial Current. The Equatorial Countercurrent is strongest at this season and the Guinea Dome most intense. Thus the upwelling off Ghana and the Ivory Coast is directly a result of the westerly winds and is totally disconnected from that in the same months in the Benguela Current. I n any case, the upwelling in the region of Pointe Noire, in Congo-Brazzaville, is in an extension of the Benguela Current, for much of the Benguela swings north-westerly at a higher latitude.

C. The Indian Ocean From April to September, the Indian Ocean is dominated by the south-west monsoon and from September to April the north-east monsoon blows. In Indonesia the south-east monsoon, which is really part of the trade wind system, is the dominant wind during the southern winter, at the same time as the south-west monsoon north of the equator. During the southern summer, there are westerly winds. Because there is such a sharp switch from one wind system to the others, the upwelling areas appear to have only slight seasonal shifts, although they are noticeable (see Table 111). There are other consequences; for example the equatorial undercurrent flows most strongly at the end of the north-east monsoon but is absent during the south-west monsoon (Knauss, 1963 ; Knauss and Taft, 1964). South of the equator, there is an eastern boundary current on the coasts of western Australia ; Wyrtki (1964) and Rochford (1962) have found some evidence of upwelling off north-west Australia from surface temperature observations. There are a number of upwellings associated with the south-west monsoon. They are in the Somali Current, off south-west Arabia, and off the Malabar coast of India. That in the Somali Current is a geostrophic upwelling caused by the tilt in the thermal structure as the current swings eastwards away from the Horn of Africa (Stommel and Wooster, 1965 ; Foxton, 1965 ;Warren et al., 1966 ; Swallow and Bruce, 1966). It is associated with the south-west monsoon only in the sense that the current flows during the period of the monsoon. Being a western boundary current it is generated by wind stress over the whole

UPWELLIhW AND THE PRODUCTION OF FISH

289

ocean as well as locally. The upwelling is limited to an area between Cape Guardafui, the eastern end of Socotra Island, 96"N 54-5"E(in the latitude of Ras Mabber about 250 miles south of Cape Guardafui), and a point on the Somali coast which shifts with season as shown in Table 111. It is possible that the biological effects of the upwelling drift seawards in the swift current (Ryther et al., 1966). Further particular distributions are given by Swallow and Bruce (1966), Warren et al. (1966), Stommel and Wooster (1965), and Foxton (1965). All the data are summarized for wind, surface temperature and salinity, nutrients and some biological observations in Wooster et al. (1967) for the north-west Indian Ocean. The areas given in Table I11 are estimated from the latter publication. Off south-west Arabia there is another coastal upwelling induced by the south-west monsoon. The oceanographic data given in Wooster et al. (1967) show that upwelling ceases at the entrance of the Persian Gulf, but suggests a slight effect on the coasts of Baluchistan during the same period. This is supported by the work on primary productivity in the area during the Indian Ocean Expedition by the "Anton Bruun " (Ryther et al., 1966) showing intense production spreading across the Arabian Sea to the coasts off Pakistan. The cruise on H.M.S. " Owen " in the same area shows upwelling and phytoplankton production in April and May off Karachi (Lee, 1963). The same survey shows a biological boundary much farther to seaward than suggested by the oceanographic data quoted above, as might be expected. The areas in Table I11 were from Wooster et al. (1967). The work of Ryther et al. (1966) shows high carbon production in a wedge north-west of Madagascar and some patches on the African coast at the southern end of the Mozambique channel. The wedge north-west of Madagascar is presumably related to the divergence between the Somali and Agulhas Currents (Ivanenkov and Gubin, 1960) as they split away from the two equatorial currents. During the south-west monsoon a southerly current is generated, with a thermocline tilt along the Malabar coast of India. The upwelling is a very shallow one originating from perhaps 20 m (Darbyshire, 1967), but the surface water is 6°C cooler than elsewhere. During July to October, low salinity water spreads over the surface from the rivers and it is at this period that the peak algal production occurs (Subrahmanyan and Sarma, 1965). During September and October, the post-monsoon period, there is a true wind-induced upwelling between Alleppey and Guilon, off Cochin, and a countercurrent is developed at 75-100m (Rama Sastry and Myrland, 1959). The situation off the Malabar coast is complex and probably the production is relatively high, as indicated by

290

D. H. CUSHINQ

the presence of phosphatic deposits offshore (Tooms, 1967); see Fig. 19a, p. 321. It is clear that upwelling extends from Trivandrum near the southernmost point of India as far north as Panjim, about 300 miles south of Bombay, but because of its nature and shallow origin the areas of upwelling cannot be estimated with quite the reliability used in the other areas. It is possible that the extent of phosphatic deposits indicates the region of upwelling as well as any other method at the moment. Carruthers et al. (1959) studied the upwelling off Bombay during the north-east monsoon and showed that the minimum oxygen layer is entrained inshore t o rather shallow water ; some evidence was produced that animals avoid the poor-oxygen water. Banse (1968) has examined theupwelling system along the whole coast andshows that an oxygen deficiency can indeed occur below the thermocline during the upwelling period and catches of demersal fish are reduced in zones of low oxygen tension (40°) are shown both in the north and south. Off California, the coastal upwelling is shown as the region of divergence in the California Current south-west of Baja California. The upwelling area off Peru from Arica northwards is shown clearly, as is the great area of divergences in the eastern tropical Pacific between the two equatorial currents, the California and Peru Currents. Along the equator and a little to the north are shown the divergences of the South Equatorial Current ;from 140"W to the Galapagos Islands the higher production above the Cromwell Undercurrent is clearly delineated. There are areas of high production off New Guinea and the Philippines as well as between New Zealand and eastern Australia. Not only is the whole area of the Alaska gyral apparently highly productive, but so is the area off Japan and to the south-east of it. There is no direct evidence of upwelling in the Kuroshio, but the production between 25"N and 40"N appears to be as high as it is in the eastern Pacific at the same latitudes. In the Atlantic, there are some observations on the African coast, mainly from the " Galathea " Expedition. There are a few observations in the two southern areas of the Canary upwelling during November on that expedition, but recently Corcoran and Mahnken (1969) have published observations off Senegal in July and August, in the Guinea Dome and off Ghana during the same period. Again, recently Lloyd (1970) has published observations from the Canary Current proper off Cape Blanc during the upwelling period. Nellen (1969) has also published radiocarbon observations from the west African area. The Canary Current appears to be a rich area, comparable to that off southern Arabia or Peru in intensity (gC/m2per day), if not as extensive or as enduring as the latter. An unexpectedly rich upwelling is that off Ghana, equally as intense as the major upwellings, for a few months in a rather small area. The Guinea Dome is extensive, but the production is not so intense as in the coastal upwellings. I n the Benguela Current there is adequate coverage in all four regions during the period December to January, sampling the main period of upwelling, but the season is more extensive than this in some parts of the region ;the mean values have been ascribed to the whole season. In the Indian Ocean, observations from the " Vityaz " and the "Anton Bruun " cover the Somali Current, the southern Arabian upwelling and the Madagascar wedge. The observations in the western half of the Arabian Sea are summarized by Wooster et al. (1967). A

297

UPWELLING AND TEE PRODUCTION OF FISH

30"

60"

90"

120"

Fro. 14. Distribution of radiocarbon measurements in the Indian Ocean, in $/ma per day (Kabanova, 1968). (1) no observations; (2) c0.15; (3) 0.16-0.38; (4) 0-380.75 ; (5) 0.75-1.45 ; (6) > 1-46 $/ma per day.

298

D. H. CUSHING

large number of radiocarbon measurements were made during the International Indian Ocean Expedition, which have been reported by Kabanova (1968); her Fig. 1 shows that there are observations in all areas. Figure 14 shows the distribution in the north-east monsoon (above) and in the south-west monsoon (below). During the north-east monsoon there is high production off Sangor Island, the Orissa coast and between Burma and the Andaman 1sla.nds in the Bay of Bengal, and off W. Ceylon. It is surprising that there are points of production on the Orissa coast during the north-east monsoon; Lafond (1957) pointed out that there was upwelling on this coast during the southwest monsoon. I n the southern winter, there is high production off the southern islands of Indonesia and on the north-west coast of Australia and off north-east Madagascar. Kabanova also examined the surface radiocarbon measurements and found that intense production occurred off the Malabar coast of India, which extended seawards for a considerable distance. Figure 14 shows the distribution of radiocarbon measurements in the photic layer during the south-west monsoon. Prominent is the intense production in the Somali Current and off southern Arabia, again extending to seaward for a considerable distance. The production off north-west Australia remains fairly high, as does that south of Java. An unexpected result is the rich band of high production off the eastern coasts of South Africa, in the Agulhas Current, which is a western boundary current, where upwelling does not take place : Burchall (1968a, b) has shown that the zone of high production lies inshore of the main axis of the Agulhas Current. However, there is moderately high production up to 500 miles offshore (Mitchell-Innes, 1967 ; Thorrington-Smith, 1969). Another interesting point is that the undercurrent at the equator does not appear at all in the radiocarbon distributions, as it does in those in the Pacific (Fig. 13). In the Indonesian area including the South China Sea, there are observations from the “ Galathea ” Expedition and a number of others, summarized by Angot (1961). The Japan Science Council, National Committee for IIOE (1966) has summarized some observations in detail off Java and off north-west Australia which have been used here. There are also observations in each of the Flores, Banda and Arafura Seas, off Vietnam and in the Gulf of Thailand which are also reported by Kabanova. The most important areas in the h d i a n Ocean and in the Indonesian region, including the South China Sea, are those off Somalia and southern Arabia, which are comparable in intensity to any upwelling area in the world. But they are somewhat smaller and endure for rather shorter seasons than the four major upwelling areas. The Orissa coast has only been explored lightly during the south-west monsoon and probably is

tTPWELLM0 AND THE PRODUCTION OF FISH

299

underestimated as a productive area. The region between Burma and the Andaman Islands appears to be fairly rich during t'hc north-east monsoon, whereas that off the Malahar coast of India may be as rich and nearly as extensive as that off southcrn Arabia. The production off Ceylon and off north-west Australia appears to take placc in both seasons, but there is not enough information to extract a seasonal trend (the same effect would appear in any of the major upwelling areas if classed by winter and summer). The Vietnam upwelling, like that in tlic Gulf of Thailand, is a minor one, but both are quite intense. The domes off Java and Sumbawa are, like the others, of rather low intensity. Those in Indonesia are of moderate productivity, as might be expected from the obscurity of the physical description of upwelling there (Wyrtki, 1961). I n Table I V the radiocarbon observations are classified and averaged by the upwelling areas. The observations by the areas and period sct out above are expressed as a single average for the upwelling area. Treating the sampling as adequate in each region the area in km2 is given within the duration of the upwelling in days; the production of carbon in each upwelling area is then given as tons C.lOs/year. The figures have then been rounded off to the levels of 3, 5, 10, 15, 35, 75 and 100 tons C.106/year. The annual production as tons Clyear is that which occurred during the upwelling season. The assumption that nothing is produced in periods outside the upwelling seasons is unjustified, but the annual rate expresses differences between upwcllirig areas which are really between the lengths of the season. From Table I V it will be seen that the differences in gC/m2per day are less than those in tons C.106/year. This is really only to be expcctcd, because the differences are due to areas and length of season. The Indian Ocean upwellings are less important than the four major upwellings because the season is usually limited to one monsoon-but the steady persistence of the monsoon winds makes the south-west Arabian area, at least, more important than, for example, the Californian area. Confidence limits have not been calculated for each area, for two reasons : (1) there are not enough observations to establish seasonal trends which are important in some areas ; (2) in some areas, e.g. the Canary Current, the Bay of Bengal and in some parts of the Indonesian area, observations are few. However, with the exception of those observations off Orissa during the south-west monsoon there are enough observations to establish fairly reliable means. The importance of the upwelling areas may be estimated by classing them as: (1) >75.10s t C/year, (2) 30-75.106 t C/year, (3) 6-30.106 t C/ year. In the first group are found the major southern upwcllings in the

308

b. #. CUSHINU

Peru and the Benguela Currents. The figure of 278.106tons C/year in the Benguela may not differ much from that of 155.106tons C/year in the Peru Current, but both are markedly different from the figures of 30. loe tons C/year in the California Current and 35.lo6 tons C/year off southern Arabia. It will be seen that the production in the Canary Current amounts to 139.106tons C/year, but that the bulk of it is based on the recent small number of observations made by Lloyd (1970)off Cap Blanc. However, it is certainly likely that the Canary Current is in the second group, comparable to the California Current and the south-west monsoon off southern Arabia, even if subsequent observations do not confirm its possible place in the first group. The intermediate areas are the California Current, the southern Arabia upwelling, that off the Malabar coast of India, and those off Chile, New Guinea, Java and Vietnam. The minor upwellings are those in the Somali Current, the Costa Rica Dome, the Guinea Dome, the Java Dome, the Gulf of Thailand, the north-west Australia upwelling and those in Indonesia, in the Banda, Flores and east Arafura Seas, the Madagascar wedge and off the Indian coast of Orissa. The greatest production takes place in the eastern tropical Pacific and in the area of the Marquesas divergences, but the intensity in both regions is low over a very broad area. Because both areas are in the open ocean, where the only present fish catch is tuna, they are not comparable with the true coastal upwellings, from the point of view of fish production. So a rich upwelling which yields high fish stocks is to be quite intense (in gC/m2 per day) over a fairly extensive region for long periods; it is this which distinguishes the Peru and Benguela upwellings (and perhaps that in the Canary Current) from all the others. The point may be made in another way, by comparing upwellings by intensity only. The first group (> 1 gC/m2 per day) comprises one subarea in each of the Peru and Canary Currents and two in the Benguela, the southern Arabia upwelling and those off Vietnam and in the Gulf of Thailand ; the difference between the first three and the latter three is really in the extensive areas and long seasons in the major upwelling areas. A second group (0.3-1.0gC/ma per day) includes one subarea from the Peru Current, three from the Canary Current and one from the Benguela Current, the Somali Current, the Guinea Dome, the Madagascar wedge, the Orissa coast, the Java coast, the coast of west Ceylon and the three Indonesian areas, the Banda, Flores and east Arafura Seas. The third group (5.0. lo6 tons C/year) is found in the three major upwellings Peru, Canary and Benguela and this arbitrary level is not found outside them. It appears that the Canaq Current is not so rich in zooplankton as the other two (c. 10. lo6 tons, as opposed to 17.106 tons in the Peru Current and about 20.106 tons in the Benguela Current). The quantity of carbon in the California Current ( 5 . lo6 tons) is considerably less. It is possible that the major upwellings in the southern hemisphere are richer than thos6 in the northern hemisphere, as was suggested from the radiocarbon measurements. I n terms of secondary production, the upwellings in the Indian Ocean or in the Indonesian area are less productive (1. lo6 or 2. lo6 tons Clyear), mainly because the areas are smaller and more limited in season. The production in the Costa Rica Dome appears t o be very high, but this is because production continues for most Qf the year. I n columns N , and N , are given the transfer coefficients, the ratios

of secondary production (in columns M , and M,) to primary production (in column D ) . Taking those in column N , , which are the simplest ratios, they range from 34-23.9%, with a mean of 12.4%. Slobodkin (1959) has presented evidence that the average figure should be about lo%, whereas Steele (1965) thinks that ecological efficiency should be higher, so long as the greater proportion of transfer occurs amongst young and very efficiently growing animals. The sources of data are very varied, in quality and in numbers of observations, and the correspondence of the transfer coefficients to expected values is a measure of the reliability of the radiocarbon measurements and the estimates of secondary production. It should be recalled that some estimates are based on Hentschel's counts from water samples, on the " Meteor " expedition (1933), and that nets of many different designs have been used. Perhaps they all catch zooplankton well enough for our present purposes and perhaps the present doubts on the efficiency of zooplankton sampling, is, in a simple-minded way, misleading. Further, the assumptions that the loss of nauplii is balanced by gain of algae and that the proportions escaping are small are roughly justified.

C. The production at the third trophic level The composition of the third trophic level in the sea is not completely known. There are predatory copepods and a large number of other planktonic predators and there are also plankton-eating fish, mainly clupeids. So, the secondary production as estimated in Table IV includes carnivorous copepods, arrow worms, jelly-fish, ctenophores, etc., which are really in the third trophic level. Excluded are the plankton-eating fish and molluscs. Very little is known about the abundance of squids and, since they are in economic and fishery terms comparable t o fish, they will be treated as such. The simplest way of estimating the tertiary production is to take 1% of the primary production and 10% of Dhe secondary production, both in carbon. Column 0 in Table IV gives the first, and columns P, and P, give the two estimates (for continuous and intermittent upwelling) from the second. If columns D and M , are compared, it will be seen that they are correlated (Fig. 15A) (r = 0.77, P < 0-01); the regression of the radiocarbon on the secondary production estimates the average transfer coefficient. The two estimates proceed from independent ones of primary and secondary production and it is assumed in both that there is a 10% efficiency between secondary and tertiary produetion. They are therefore not entirely independent, but the degree of correlation between them suggests that the basic methods are sufficient for our present purposes.

UPWELLING AND THE PRODUCTION O F FISH

307

It is likely that the best estimate of tertiary production lies between that derived from the primary production and that from the secondary production. So column Q1 represents an average of the estimates in columns 0 and P, and column Qz represents an average of those in columns 0 and P,. I n columns R, and R,,these estimates of tertiary carbon are put into wet weight. Vinogradov (1953), in his Table 284, shows that the average water content of plankton-eating fish is about 70% and he also shows in another part of his paper that 45% of the dry weight of such fish is composed of carbon. So, a carbonlwet weight ratio of 13.5% was used and so the figures in columns Q, and Q, were raised by 7.47 to give the figures in columns R, and 8,.I am grateful to the late Dr. M. B. Schaefer €or pointing out to me that the ratio of carbon to wet weight used in Gushing (1969, restricted), although perfectly applicable to copepods, is not applicable to fish. The total weights (excluding the eastern tropical Pacific) are 691.2-786.5 tons. lo4 carbon/year or 51.64-58-74 tons. lo6 wet weight/ year. The estimates from the eastern tropical Pacific and from the Marquesas divergences are excluded because the oceanih production cycle has a third trophic level of very small fish, for example, the myctophids of the Deep Scattering Layer. At the present time, it is assumed that these fish will not be exploited because they are widely dispersed and costly to catch. So the sum of the tertiary production available in coastal upwellings (as opposed to equatorial ones) is about 50-60 million tons wet weightlyear. If the true transfer coefficient of energy is higher, say 15%, then the tertiary production would amount to 75-90 million tons (if the higher transfer coefficient applied to one transfer) or 112-135 million tons (if the higher transfer coefficient applied to both transfers). So three estimates are available : Transfer coefficients Tertiary production (M tons wet weight)

(0.10)2 55

(0-10.0-15) 83

(0.15)' 124

It must be recalled that a proportion of the secondary production as calculated is composed of predators and the postulated trapsfer coefficientsmay be set as 0.09 or 0.135. Then our figures are : Transfer coefficients Tertiary production (M tons wet weight)

(0.09), 50

(0.09.0-135) 75

(0-135), 112

The planktonic tertiary production has not been added to these figures because we are interested in the production of fish, whigh, for present purposes, includes pelagic molluscs such as squid. However, in Fig. 15b A.M.B.--g

11

308

D. H.CUSHINGI

some evidence is presented to show that the first transfer coefficient (primary to secondary production) may be less than 10%. We have no information on the second transfer coefficient, except that Steele (1965) suggested that it was high in temperate waters. Perhaps the nearest approach to the truth is 75 million tons (0.09.0.136).

''1

0

A

10

-0

.t

g 8 u e

'-

H '

8

0

6-

w a

0

//

5-

'/

0 '

/

c

I

0

10

20

30

1

1

40 50 60 70 80 90 100 Carbon (tons 106/year primary production)

1

1

110

120

*Corm R i a Dome

2o

B

0 Guinea

California 2

m8engusla 2 Somali *Peru 2 Benguela 4

0

I

I

I

I

0.5

1.0

1.5

2.0

g C/m2/d primary production

FIG.16. (A) Relation of secondary production to primary production. (B) Dependence of transfer coefficient on the intensity of primary production (in @/ma per day).


309

If we compare the tertiary production by upwelling areas, we find that the Peru and Benguela Currents are the richest (12 and 18 million tons wet weighflyear respectively), followed by the Canary Current (8 million tons wet weight/year) and the California Current (3 million tons wet weightlyear). The Indian and Indonesian upwellings are much smaller, generating 1-2 million tons wet weight/year each. Howcver, if we add them together and take into account the poor sampling of upwellings in the area, a possible figure of 5-10 million tons wet weight/ year emerges as a total for the Indian Ocean and Indonesian region. If the tertiary production is taken as being composed of fish and squid, then the annual production is the annual increment t o populations in recruitment and in growth. It is assumed that the maximum biomass of a fish stock is reached during adult life, because from one generation t o the next, the weight of gonads must increase by three to six times t o create the filial stock. Fish in subtropical areas do not appear t o live very long ; Peruvian anchoveta live for 2 or 3 years and Californian and South African sardines live for 3 t o 6 years (Davics, 1958; Marr, 1960). Hake, which feed on euphausids, may live somcwhat longer. A rough effective lifcspan in the fishery of about 3 years would be a reasonable estimate for all fishes. Hence, the stocks available in the upwelling areas might range from 150-340 million tons wet weight ; the yield t o all consumers of the tertiary production, of which man can probably take only half, may be equivalent t o a little more than one year’s recruitment. I n the Californian Current, it was shown that the sardines and anchovies, together with the hake, predominated. The figure of 3 million t,ons/ytar is not unexpectcd from our knowledge of the sum of the sardine or anchovy stock and the hake stock. According t o Ahlstrom (1969), about half the fish population consists of anchovies and about one-sixth of hake ; thus the annual recruitment t o the anchovy population might be as much as 1.5 mJlion tons and that t o the hake as much as 0.5 million tons. If the anchovy lives 3 years in the fishery, the unexploited stock might amount t o just over 3 million tons (allowing for a natural mortality of 33% (Clark and Marr, 1955)). If hake live 6 years in the adult stock, then it would amount t o just less than 2 million tons, allowing for a natural mortality of 20%. The tertiary production in the Peru Currcnt amounts t o 12 million tons and the anchoveta outnumbers all other species in the egg collections by a factor of ten. If they live in the fishery for 2 years then the total stock amounts to 24 million tons, and the prescnt annual catch is of the order of 8-10 million tons. Gulland (1968) has suggested that the total annual deaths (equal t o total annual production) amount t o 18-20 million tons,

310

D. H.

uusma

which is rather greater than the estimate of 12 million tons. However, there is some correspondence between the stocks as estimated by the present very rough method and those estimated by the techniques of population dynamics.

D. The transfer coeficients Steele (1965) has suggested that ecological efficiencies might be considerably greater than 10%. I n the upwelling areas, where populations increase by many times between generations, growth is less important than survival. When survival is high during periods of plentiful food, the population rises, and when survival is low during periods of food 1 lack, the population declines. Steele suggested that if herbivores in- , creased under conditions of plentiful food and were themselves eaten when they stopped growing, ecological efficiencies of up to 25% might be expected. The transfer coefficients used here are not strictly estimates of ecological efficiency, because they are ratios of production rather than ratios of yield. The average coefficient is 12.4%. Because the production cycle in an upwelling area is possibly a temperate one, the populations of herbivores are increasing ones and so the somewhat higher transfer coefficients are not unexpected. Given the increase in transfer coefficient with abundance, the correlation shown in Fig. 15A is fitted by a linear regression (r = 0.77, P < O - O l ) , shown as a full line. But the variance increases sharply with abundance, because differences in abundance form a geometric series. The estimates of primary production are as good as the estimated averages and the estimated lengths of the upwelling seasons ; the estimate of secondary production appears t o be roughly as good as that of primary production. A straight line drawn through the origin and the mean does not fit the data so well, which suggests that the best fitting line would be slightly curved, in a convex manner. This would suggest that the transfer coefficient decreases with increased primary production. It is the reverse of the conclusion in Gushing (in press) which was based on limited data from the Pacific Ocean. Another relationship is that between transfer coefficients and the intensity of primary production (gC/m2 per day), which is shown t o be markedly inverse; it appears that a greater proportion of material is lost in transfer at high intensities. The transfer coefficients tend to be lower in the upwelling areas, which means that they are relatively inefficient. I n effect the coastal upwellings are compared in Table I11 with the offshore divergences. Where the intensity of primary production is low ((0.5 gC/m2per day) in the offshore divergences, the transfer coefficient is high, where

UPWELTAXNOAND THE PRODUCTION OF FISH

31 1

herbivores have to search to some degree for food. Yet where they do not have t o do so in the coastal upwellings themselves, the transfer coefficients are lower. Perhaps some form of superfluous feeding takes place in the rich areas, as Beklemishev (1957) suggested. Algae and herbivores are drifted out of the upwelling areas. But the fish populations are retained within the coastal upwelling areas and so provide a means by which the energy of the transitory plankton populations is extracted. In temperate seas, the abundant fish stocks tend to spawn at a season and position which allows the larvae to exploit the food available in the production cycle. In the tropical and subtropical seas, the abundant fish stocks have located themselves in the coastal upwelling areas and exploit the production cycle there as it passes through.

VII. THE BIOLOGYOF AN UPWELLING AREA Wooster and Reid (1963) have estimated the Ekman offshore transport by 5' sectors and by quarters of the year according t o the wind stresses. Their figures show that the offshore transport was most intense in winter in the Peru Current and for most of the year between Liideritz and the Orange River in the Benguela Current. In the Canary Current the highest values in spring and summer are about two-thirds of those in the two southern currents and a little more than twice that in the California Current. This order (Peru, Benguela, Canary, California) is that observed in total primary production and in total secondary production and so in a very general way the production of living material is dependent upon the rate of upwelling. But there is no correlation between the Ekman transports (which are roughly assumed to be related to the rate of upwelling) and the intensities of primary production, in gC/ma per day, or the stocks of zooplankton, in ml/l 000 m3. The Peru Current upwelling has a high total production in plants and animals because it lasts a long time, but the intensities in gC/m2per day and the zooplankton stocks appear to be low. Strickland et al. (1969)have published four radiocarbon observations from " brown water '' off Pisco, and their average value amounted to 2.4 gC/m2 per day, which is considerably greater than the average of 0.67 gC/m2 per day; however, there are only a few observations and many have been taken in the upwelling water ;indeed only a few patches of brown water were found by Strickland et al. in upwelling water. The Peru Current upwelling and that in the California Current were sampled by the same equipment, by the same people at about the same period: but there is no difference in the radiocarbon measurements in subarea 1 in the Peru system and all three subareas in the California

312

I). H.UUSHlXU

Current system (on Table 111),or in the stocks of zooplankton in the whole current system, between the two areas, despite a difference of three times in the Ekman offshore transport. The simplest view of the upwelling production cycle is t o consider it as starting at the bottom of the photic layer and continuing as the water rises. The quantity of plants and animals in the water below 200m must be low and as a consequence, the production cycle in an upwelling area resembles that in temperate areas rather closely, because that also is a discontinuous cycle. Heinrich (1961) has suggested that the average generation time in the upwelling areas is about 40 days, so effective grazing should start about 20 days after the start of upwelling. The photic layer may be up t o 50 m deep and the rate of upwelling might be 1, or exceptionally, 5 m/day, so the peak of the production cycle should occur at or near the surface, at or near the line of upwelling. A more complex situation occurs if the plant production becomes vulnerable t o mixture of zooplankton generated by earlier productions. Consider production in the rising water, without grazing. From Steele and Menzel (1962),

P

= aIoexp(-kZ

- 2 exp(-kZ))

(1)

where I,,is the average radiation at the surface in ly/d ; where 2 is the depth in m ; where k is the extinction coefficient ; where a is a constant (= 0-48) ; where p is the daily production in gC/m3 per day. Steele and Menzel's average figure of 180 ly/d for the Sargasso Sea has been used ; a value of k = 0.1 has been used, as an average ignoring its increase with increasing production. Let Zp be the depth of the photic zone, hence 2 = zp - wht,

(2)

where W,is the ascending velocity in m/day. Between time t and t 6t

+

P6t = aIoexp(-[k(Zp - Wht)

+ 2 exp[-k(Zp

- Wht)]]}st,

then the total production, in gC/m2 per day, as water rises from the bottom of the photic layer (2 = 2 p , t = 0) to the surface (2= 0, t = z p / W h ) is

UPWELLING AND TEE PRODUCTION OF FISH

313

- a10

[exp-2 exp(-kZp) - exp( - 2 ) ] 2k Wh I am grateful to my colleague, Mr. J. G. K. Harris, for the development of equations ( 2 ) t o ( 5 ) . Figure 16 shows the relation between total production during ascent (for a photic layer of 20 m and for one of 100 m) and the ascending velocity. Ignoring grazing, the slower the upwelling velocity, the

Fro. 16. Relation botween total production, p. during ascent and ascending velocity. Wh, (in m/day), for two depths of photic layer (20 m and 100 m).

greater the production during the ascent, irrespective of the depth of the photic layer. From Fig. 16 an upwelling velocity of 0.5 m/day will yield a production cycle which generates its own grazing capacity at the surface, if grazing became effective after 20 days (with a photic layer of 50 m in depth). A greater upwelling velocity, irrespective of the depth of the photic layer, means that the production has not gone on for very long (less than half a generation) when i t reaches the surface. There the water moves away rather more quickly than it rises and so the production might become vulnerable to additional grazing from animals produced earlier which have drifted offshore. Perhaps the faster rate of upwelling off Peru modified the production cycle in this way to some extent, leading t o rather lower standing stocks than expected.

314

D. H. UUSRINQ

Less important than the particular point of the data in the Peruvian upwelling is the possibility of developing a dynamic model of u p w e b in biological terms. It would be quite easy to put a grazing term in the equations given above, if information were available on generation time of the herbivores of a more extensive character than that used in the present paper. All estimates of upwelling velocity have been obtained indirectly and no measurements have yet been published. So the model developed above can only be used in model situations, unless sufficient reliance be placed on the biological variables to use it to obtain direct estimates of the upwelling velocity. Figure 10 shows the gradual decay in quantity of living material from the shore in an upwelling area. I n general Thrailkill’s cha* Station numbers

I I

131

130

129

128

I

I

I

I

Very dispersed

I

Dispersed

IVery

127 I

28

29

30

31

I

1

1

I

Dense

dense

FIG.17. The distribution of echo-traoes in the thermocline off Peru (Flores end Efiw 1967).

of average zooplankton volume show a, decline of perhaps fXty times in 300 miles. The true path of the water will have a large southerly component and so such a decline may really occur in a much greater distance. Although the true path is unknown it is likely that the period of decay may be 20-50 days, not very different from the time it took the water to rise. So we have a picture of a production cycle of the same period and amplitude as that found in higher latitudes, but arbitrarily split by the upwelling process into two parts, that in the rising water and that in the water drifting away from the shore. The fish in an upwelling area are distributed in a particular way. Figure 17 shows echo traces at the thermocline in the Peru Current upwelling. They are probably anchoveta and they live in the upper part of the thermocline and presumably migrate towards the surface at


315

night. On the bottom live flatfish in rather shallow water, and near the bottom in deeper water live hake and rosefish. The hake probably migrate upwards at night and feed on euphausids. Between the anchoveta and the hake live the horse mackerel, possibly in the lower parts of the thermocline and below. At the surface live guano birds which are surprisingly abundant. I n the Peru Current, thcre are 30 million birds, mainly pelicans, boobies and cormorants ;during El Niiio, the numbers are sharply reduced, because some migrate southwards out of the area when the fish are no longer accessible and some die of starvation. I n 1958, during El Nifio, the bird populations were sharply reduced, but by 1962 the numbers of birds had fully recovered. So they must eat very large numbers of anchoveta. In the Benguela current, Davies (1958) has estimated that the cormorants off SouthWest Africa take 1 000 tons of horse mackerel and 6 000 tons of pilchard, that the gannets (or boobies) take 5 000 tons of horse mackerel and 16 000 tons of pilchards, and that the penguins take 1 000 tons of horse mackerel and 21 000 tons of pilchards. It is no accident that in many of the upwelling areas there is a Cab0 Blanco, Cap Blanc or Cape Blanc. In addition to the birds there are tuna-like fishes and whales. Nakamura’s (1969) atlas of the catches of tuna by the Japanese longline fleet is really a chart of the divergences in the oceanic subtropical anticyclones. But the coastal upwellings are less important to the tuna than the offshore divergences : it is no accident that the eastern tropical ocean, particularly the eastern tropical Pacific, is an important area for tuna fishermen. Although tuna may be caught in the area of coastal upwelling, it is likely that they pass 100 km or more offshore. The community of fishes in an upwelling area is a specialized onc, as pointed out earlier, with some analogies to a temperate community of fishes. The fish characteristic of an upwelling area are not caught much outside i t ; hake occur between Cape San Lucas and Kodiak Island, according to Alverson and Larkins (1969), but their area of abundance is the California Current upwelling system. The possible dependence of hake upon the current/countercurrent system has already been noted. The Californian sardine spawns right in the coastal upwelling zone, as physically defined ; indeed the points of upwelling, south of Point Conception, off San Diego and off Punta San Eugenio, are recurrent centres of intense spawning (Ahlstrom, 1966). The Peruvian anchoveta spawns between Punta Aguja and San Juan in late winter to early summer when the Ekman transport is most intense (Wooster and Reid, 1963) and the greatest densities of eggs are found within 100 km of the coast (Flores, 1967 ; Flores and Elias, 1967) where the radiocarbon values are highest (Forsbergh and Joseph, 1964). So the Californian sardine and

316

D. H.UUSHING

the Peruvian anchoveta spawn near the line of upwelling along the shore. There is sometimes a very narrow coastal countercurrent during the season of upwelling both off California (Reid et al., 1958) and off Peru (Wyrtki, 1963). Because the fish live in the upper half of the thermocline, the countercurrent below 200m is of little use t o them. But here is a mechanism by which the fish can move towarde the pole during the upwelling season, and the Californian sardine in its period of abundance was caught as far north as British Columbia late in the season (Marr, 1960). Thus the major components of the community of fishes, the sardine (or anchovy) and the hake, may well have a system of retaining themselves within the upwelling area merely in the two current/countercurrent systems.

86" 10

83"

80"

71"

74"

71"

3"

6"

9"

12"

15"

18" 20" FIG.lS(8). The distribution of zooplankton in ml/haul displacement volume (Flom, 1967 ; Guillen and Florea, 1967).


317

There is a remarkable phenomenon in the Peru Current upwelling. Figure 18 shows the distribution of zooplankton and that of anchoveta eggs at the same time (Flores, 1967 ; Guillen and Flores, 1967) ; it will be seen that the spawning anchoveta, a8 shown in the egg distributions comprising 90-95% of all fish eggs sampled (Flores, 1967), appears to exclude the zooplankton. The inverse correlation is not spatially exact, which may suggest a time lag in its generation. Like other anchovies, the Peruvian anchoveta traps algae on its narrow gill rakers, but there is some evidence that it feeds on smaller copepods (Villanueva et aE., 1969). Then the apparent exclusion of zooplankton by the anchoveta may have occurred because the fish stripped the water of herbivores. This would mean that the fish concentrate for spawning and tem-

B 1-100 101-500 ,500

2oo FIQ. 18(b). The distribution of anchoveta of the coast of Peru, in numbers/haul with a Hensen net (Flores, 1967 ; Guillen and Flores, 1967).

318

D. H. UUSHING

porarily reduce the herbivore numbers considerably, but that the herbivores would recover after the fish had dispersed ; since writing this I have found that my colleague, A. C. Burd, who has worked in Peru, has come to the same conclusion. Thus it appears that the anchoveta can temporarily play a controlling part in the production cycle ; one is reminded of the part possibly played by pilchards in the production cycle in the English Channel (Cushing, 1961 ; Russell, 1936). If the numbers of herbivores are drastically reduced, the algal numbers should increase in the surface water after the spawning of the anchoveta ; light and nutrients should be available in excess and, with the grazing restraint removed, a second algal outburst should occur and it is quite possible that it is unrelated to the processes of upwelling. This short account of the biology of an upwelling area listed four subjects : a rough model of the production dynamics of upwelling, the vertical and community structure of the system, the possible mechanism by which the fish stocks remain contained within the area, and the important part played by the anchoveta in the very simple production cycle of an upwelling area. The four are obviowly linked in that they are all parts of a single ecosystem. I n this sense an upwelling area can be studied as a biological unit, as many people have studied temperate production cycles. Few of the latter have been linked to the fish stocks partly because, in temperate seas, the connection between fish stock and production cycle is not readily made. This is because fish are often caught at points distant from the region of larval drift (between spawning ground and nursery ground) and so the ecosystem becomes artificially split into separated studies. I n an upwelling area the parts of the ecosystem coexist and can be studied as a whole with present techniques. VIII. DISCUSSION There are three ways of briefly charting the world's upwelling systems. The most obvious is the chart of phosphatic deposits (Fig. 19A; Tooms, 1967). The four major upwelling systems are shown clearly ; that in the California Current is continuous from the Mexican border to the coasts of Washington State. The lack of deposit off Baja California suggests that the present area of upwelling off Punts San Eugenio is aberrant and the recent southerly movement of upwelling since 1949, referred to above, may be an aberration over a geological time period. The Peruvian upwelling appears to be no different from its present distribution, except that there is no break south of Arica. The Canary Current deposits are split at Cap Blanc, but they do not extend south of Dakar as does the present upwelling area. The Benguela Current deposits do not appear to extend very far north of the Orange


319

River, but do extend for a considerable distance eastward of the Cape of Good Hope. Of the lesser upwellings those off Somalia, southern Arabia, the Malabar coast of India and off the southern coasts of Ceylon are shown ; of these, the Somali upwelling, like that south of Ceylon, appears t o have generated more extensive deposits than would be expected from the present extent of the upwelling areas. The deposits off Ghana correspond to the area of the Guinea upwelling, but those off north-west Australia are much more extensive than might be expected and lie west of the present upwelling area. With the exception of the last area, the phosphatic deposits show the presence of the major upwellings and the intermediate ones, but not the minor ones or the equatorial ones. Figure 19B shows the distribution of guano islands (Hutchinson, 1950). There is a concentration off Baja California and in the Gulf of California, all the way down the coast of Peru, on the south-west coast of South Africa, off southern Arabia, off Somalia, off northern Madagascar, off north-west Australia, off Vietnam and north of New Guinea. The major upwelling which is not recorded by this method is that in the Canary Current. But minor ones, like those in the Flores Sea and Banda Sea, are recorded. Perhaps the method is a little too sensitive to the presence or absence of birds or suitable islands. It is extraordinary that although the upwelling off the coast of Venezuela and off Puerto Rico appears on the chart, those on the north coast of Yucatan, on the coast near the delta of the Mississippi and off the west coast of Florida are absent. The best representation of the upwelling areas throughout the world is shown in Fig. 19C; it is a chart of the positions of capture of sperm whales by Nantucket whalers between 1726 and 1919 (Townsend, 1935). In the northern summer, or southern winter, catches were prominent in the southern upwellings, in the Peru Current and in the Benguela Current, but they appeared there also in the southern summer. No catches at all were made in the California Current and only light catches were made in the Canary Current; in the northern winter, however, some catches were made off Baja California and some off Casablanca. The first was really the beginning of the Californian upwelling and the second the end of that in the Canary Current. The most prominent feature of this chart is the band of captures along the Line in the Pacific, effectively in the divergences of the South Equatorial Current ; those off the Marquesas Islands are noticeable, as are those further east. The same structures occur in the other two oceans, but for some reason they did not attract catches of sperm whales. A particular region which appears in both charts is the area north of Madagascar, the Madagascar

320

D. H. CUSHWO

Wedge. An interesting point is that the most prominent part of the sperm whale catches in the Canary Current comes from the extension of the current into the North Equatorial Current and from the Guinea Dome. This suggests that the sperm whales do not in fact aggregate in the coastal upwellings themselves but in the offshore divergences. The whales were caught off Angola and the Congo rather than off South Africa and South-West Africa ; they were caught in the Peru Oceanic Current rather than the Peru Coastal Current, in the offshore divergences of the Madagasar Wedge, in those of the North Equatorial Current in the Atlantic, and in those of the South Equatorial Current in the Pacific. Thus the sperm whale must be a truly oceanic animal like the tuna and may be excluded to some extent from the coastal upwellings themselves ;indeed they may be excluded from much of the California Current by the grey whale. There are two anomalies in this interpretation of the chart of sperm whale catches, in the North Pacific and in the North Atlantic, south-east of Japan and south-east of Nantucket. The latter may be a function of the nearness of the home port, but the former is difhult to explain, being a little too far south of the divergences of the Kuroshio extension. If the two charts, of phosphatic deposits and of sperm whale catches, were combined, the result would be a nearly complete distribution of upwellings, coastal and offshore, throughout the tropical and subtropical seas of the world. The two charts really represent two eco-

FIG.19. (A)

L

I

I

I

180'

90'

0'

90'

I

I

I

I

(C)

FIQ.19. Indirect indications of upwelling arcas throughout the world : (A) tiist,ribution of phosphatic deposits (Tooms, 1967) ; (B) distribution of guano islands (Hutchinson. 1960) ; (C) distribution of sperm whale catches from Nantucket, 1726-1919 (Towneend, 1936);above, northern s u m m e r ;below, northern winter.

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cusma

60'' I I I I I I I I FIU.2O(a). Distribution of divergences and convergences, in kg/m3/sec,in the northern winter. T h e cross-hatched meas m e divergences and the diagonally shaded m a s are convergences (after Hidaka and Ogawa, 1968).

systems, that of the coastal upwelling and that of the offshore divergences. Each coastal upwelling system is distinct from others and comprises a biological unity which may suffer little or no exchange with the ocean or with another coastal upwelling. The system of offshore divergences may have a profoundly different basis in that the animals may move from one to another. Nakamura (1969) suggests that tuna in the Pacific migrate round the subtropical anticyclone in the direction of water flow ; hence they would be expected to move from the offshore region off California into the California extension, along the divergences of the North Equatorial Current and westward. Some species of tuna may not behave like this at all, but others may well do so, which means that they subsist by moving from divergence to divergence. Figure 20 shows a simplified distribution of divergences and convergences in the Pacific (from Hidaka and Ogawa, 1958). It is possible to draw a line in

323

UPWELLING AND THE PRODUCTION O F FISH

I

I

1

I

I

I

I

I

FIQ.20(b). Distribution of divergences and convergonces, in kg/m3/sec, in tho northorn summcr. The cross-hatched areas ere divergonces and tho diagonally shadod a r o a ~ are convergences (after Hidaka and Ogawa, 1958).

the lower chart (20B) from 160°W450N round the anticyclone to 15"N180°W; similarly, in the upper chart, a line can be drawn from 15°N1800W round the anticyclone to 45"N16OoW. The first line would follow a set of divergences in the northern summer and the second a set in the northern winter, and a similar picture could be constructed in the southern anticyclone. The purpose of this speculation is to suggest that the scale of the offshore ecosystem is in fact oceanwide and continuous. In this system the production cycle is in a quasi steady state, the plankton communities are diverse, there is a third trophic level inserted between herbivore and tuna (the fishes of the Deep Scattering Layer) and tuna spawn across the whole ocean (Matsumoto, 1966). The coastal upwellings are then to be considered as aberrations. Because the production of living material extends offshore beyond the dynamic boundary, it drifts away and contributes to the oceanic system.

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Then, biologically, the distinction between coastal and oceanic systems is really in the fish populations, one group of which is retained within the coastal upwelling system and the other which passes through the divergences offshore. However, the distinctions must not be pressed too far, because Ahlstrom’s distributions of eggs and larvae show that sardine, anchovy (Ahlstrom, 1966) and hake (Alverson and Larkins, 1969), the dominant species of the Californian upwelling, are spread well beyond the dynamic boundary during their periods of abundance. I n this paper certain speculative ideas have been put forward on the nature of the production cycle in upwelling areas and on the consequences of the well-known correlation between phosphorus and zooplankton. The upwelling production cycle appears t o be homologous with that in temperate waters, in that it is discontinuous and of high amplitude, generating large quantities of living material ; indeed the community structure itself has the character of a temperate one. The correlation between phosphom and zooplankton suggests that production causes the decline of nutrients and not vice versa as was originally suggested. If the upwelling production cycle is a temperate one, one would expect that nutrients would decline on a vector offshore as they do temporarily in a temperate cycle. Then the correlation in space shown between phosphorus and zooplankton should imply that in temperate waters the quantities of phosphorus represent regenerated material, not in the early parts of the cycle, but perhaps so in the later parts of it. Then the decline of phosphorus (and other nutrients) in temperate waters is represented as a loss to plant and animal material, although the residual quantity may be all regenerated. So in the upwelling cycle, as it moves off and as the phosphorus is reduced, it is lost t o living material and what remains is regenerated. The methods used in this paper are crude, yet in those areas in which the fish production has been estimated there is some correspondence between the measures of fish production and of tertiary production. Further, the estimates of primary production were correlated with those of secondary production, from which it may be concluded (together with the correspondence with fish production) that they are quite reliable. It is extraordinary that the average intensities of production (in gC/ma per day) in upwelling areas did not differ very much, which implies that the processes, in physical terms, could be described in model terms. I n the same way, the intensities of secondary production were rather similar between the areas of upwelling, so that the alleged difficulties of estimating zooplankton in terms of sampling and in terms of patchiness do not really exist. The quantities can be properly measured and the real obstruction to the improvement of


325

estimating secondary production lies in our ignorance of the duration of invertebrate juvenile stages and the dependence of this upon temperature. Such work is not difficult and could be carried out in small marine laboratories; without such measurements, the collections of zooplankton made at sea with costly crews and expensive research ships are really of very little value. Smith's (1969) recent review of the physical studies of upwelling is notable for the demonstration that the theoretical formulations of upwelling are confirmed in general by physical measurements. Hence, some physical understanding of the processes is available and could be exploited in a study of upwelling. It is clear from the present study that the biological study of upwelling is a little primitive. An early stage in oceanographic research is expressed in the form of surveys; it is a necessary and exploratory stage which, thanks to the intensive work off California in the last two decades, is in principle complete. This does not mean that explorations, particularly in some areas, are no longer needed, but rather that the nature of the work should change t o some extent. The major change in the direction of upwelling research may be in the time interval of sampling. The best methods used so far have employed surveys of about a month apart. But upwelling is often an intermittent process, periods of wind stress alternating with periods of calm, and so the time unit of study should be as long aa a period of wind stress or a period of calm. Unless enormous resources become available, a major upwelling cannot be described at intervals of 3 or 5 days ; perhaps it should not be so described because of the potential waste of data. In other words, it might be of advantage to study a smaller area, for example, the Guinea upwelling, the area off Punta San Eugenio in California, or that off Somalia. Of course, for a short season, a major upwelling region may comprise a small enough region to make study worth while, like that off Oregon. Physical measurements can be taken by continuous recording, for example of temperature, salinity and oxygen. Measurements of phosphate, nitrate, silicate, nitrite, chlorophyll and turbidity can be made continuously with Autotechnicon methods (Armstrong, Stearns and Strickland, 1967). Similarly radiocarbon measurements can be made rapidly and reliably with scintillation counters (Wolfe and Schelske, 1967). Zooplankton hauls above 200 m and below 200 m can be made with high-speed tow nets (Beverton and Tungate, 1967), and the same gear can be used for eggs and larvae. High-resolution acoustic gear can be used at all depth strata, together with means of capture at any depth for identification. It is not of value to collect very large quantities of data unless a model of the biological

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processes is developed. Since Riley (1946 ; Riley et al., 1949) made some of the earlier models, many varieties have evolved and many methods of computer treatment have appeared.

IX. REFERENCES Abbott, D . P. and Albee, R. (1967). Summary of thermal conditions plankton volumes measured in Monterey Bay, California, 1961-1966, Rep. Calif.coop. ocean. Fkh. Invest. 11, 155-166. Ahlstrom, E. H. (1966). Distribution and abundance of sardine and anchovy larvae in the California Current region off California and Baja California, 1951-64: a summary. Spec. scient. Rep. U.S.F k h Wildl. Sew., (Fkheries), No. 634,71 pp. Ahlstrom, E. H. (1967). Co-occurrences of sardine and anchovy larvae in the California Current region off California and Baja California. Rep. Calv. coop. ocean. Fkh. Invest. 11, 117-136. Ahlstrom, E. H. (1969). Mesopelagic and bathypelagic fishes in the California Current region. Rep. Gal$. coop. ocean. Fkh. Invest. 13, 39-44. Alverson, D. L. and Larkins, H. A. (1969). Status of knowledge of the Pacific hake resourcee. Rep. Calif.coop. ocean. Fkh. Invest. 13, 2 P 3 1 . Angot, M. (1961). A summary of productivity measurement in the southwestern Pacific Ocean. I n " Proceedings of the Conference on Primary Productivity Measurement Marine and Freshwater, University of Hawaii." (M. S. Doty, Ed.) TID-7633, 1-9. U.S. Atomic Energy Commission, Oak Ridge. Antia, N. J., McAllister, C. D., Parsons, T. R., Stephens, K. and Strickland, J. D. H. (1963). Further measurements of primary production using a largevolume plastic sphere. Limnol. Oceanogr. 8 (2), 166-183. Armstrong, F. A. J., Steams, C. R. and Strickland, J. D. H. (1967). The measurement of upwelling and subsequent biological processes by means of the Technicon Autoanalyzer and associated equipment. Deep Sea Res. 14 (3), 381-389. Arrhenius, G. (1963). Pelagic sediments. I n " The Sea '' (M. N. Hill, Ed.), vol. 3, pp. 655-727. Wiley Interscience, New York. Arthur, R. S. (1965). On the calculation of vertical motion in Eastern Boundary currents from determinations of horizontal motion. J . Bwphys. Rea. 70, 2799-2804. Bang, N. (1971). The southern Benguela Current region in 1966; bathythermography and air-sea interaction. Deep Sea Ras. (in press). Banse, K. (1968). Hydrography of the Arabian Sea Shelf of India and Pakistan and effects on demersal fishes. Deep Sea Rea. 15 (l),45-80. Bayliff, W. H. (1963). The food and feeding habits of the anchoveta, Centengraulis myatiwtwr, in the Gulf of Panama. Bull. inter-Am.trop. TunaCommn, 7 (6), 399-459. Beers, J. R. (1966). Studies on the chemical composition of the major zooplankton groups in the Sargmo Sea off Bermuda. Lirnnol. Oceanogr. 11 (4), 520-528. Beklemishev, K. V. (1957). Superfluousfeeding of the zooplankton and the problem of sources of food for bottom animals. TrudG vsea. gidrobwl. Obshch. 8, 354-368.


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Berrit, G. R. (1958). Les Baisons marines B Pointe Noire. Bull. Inf. Com. cent. Ochnogr. Z h d e C6tea. 10, 335-358. Berrit, G. R. (1961). Contribution B la connaissance des variations saisonnieres dans le Golfe de GuinBe. Observations de surface le long dcs lignes de navigation. Cah. ochnogr. 13 (10). 715-727. Bcrrit, G. R. (1962). Contribution B la connaissanco dcs variations snisoiinibres dans lo Golfe de Guinee. Observations de surface lo long des lignrs do nnvigation. 26me partic. fitude regionale (suite et fin). Cah.ochnogr. 14 (10). 719-729.

Beverton, R. J. H. and Tungate, D. S. (1967). A multi-purposc plankton sampler. J. Cona. perm. int. Explor. Mer, 3 1 (2), 145-157. Bjerknes, J. (1961). " El Niiio "; a study based on analysis of ocean surface temperatures 1935-57. Bull. inter-Am. trop. Tuna Commn, 5 (3), 219303.

Blackburn. M. (1966). Biological oceanography of the eastern tropical Pacific : summary of cxisting information. Spec. scient. Rep. U.S. Fish Wildl. Sew. (Fisheriea),No. 540, 18 pp. Blunt, C. E. (1869). The jack mackerel (Trachurw, symmetricus) resource of the eastern North Pacific. Rep. Calif. coop. oceanic. Fish. Inveat. 13, 46-52.

Bogdanov, D. V., Sokolov, V. A. and Khromov, N. S. (1968). Regions of high biological and fishing productivity in the Gulf of Mexico and Caribbean Sea. Okeunologiya, 8 (3), 466478. Bolin, R. L. and Abbott, D. P. (1963). Studies on the marine climate and phytoplankton of the central coastal area of California 1964-60. Rep. Calif. coop. oceanic. Fiah. Inveat. 9, 23-45. Bowley, C., Greaves, J. R. and Spiegel, S. L. (1969). Sunglint patterns: unusual dark patches. Science, N . Y . 165, 1360-1362. Burchall, J. (196th). Primary production studies in the Agulhas Current region off Natal-June 1966. Inveat. Rep. S . Afr. Ass. mar. biol. Rea. 20, 16 pp. Burchell, J. (196813). An evaluation of primary productivity studies in tho Continental Shelf region of the Agulhas Current near Durban (1961-66). Inveat. Rep. S. Afr. Ass. mar. biol. Rea. 21, 44 pp. Buys, M. E. L. (1959). The South African pilchard (Sardinops ocetlata) and massbanker (Trachurue trachum)-Hydrographical environment and the commcrcial catches, 1950-57. Inveatl Rep. Div. Fish. U n . S . Afr. No. 37, 559732.

California, Department of Fish and Game. Marine Research Committoo (1952). Prog. Rep. Calif. coop. Sardine Rea. Progm, 1951-52, 61 pp. California, Department of Fish and Game, Marine Research Committee (1953). Prog. Rep. Calif. coop. ocean. Fish. Inveat. 1952-53, 44 pp. California, Departmont of Fish and Game. Marine Research Committee (1958). Prog. Rep. Calif. coop. ocean. F b h Invest. 195668, 57 pp. Carruthers, J. W., Cogate, S. S., Naidu, J. R. and Laevastu, T. (1959). Shorewards upslope of the layer of minimum oxygen off Bombay : its influencc on marine biology especially fisheries. Nature, Lond. 183, 1084-1087. Clark, F. N. and Marr, J. C. (1955). Population dynamics of the Pacific sardine. Prog. Rep. Calif. coop. ocean. Fish. Inveat. 1953-55, 12-48. Copenhagen, W. J. (1953). The periodic mortality of fish in the Walvis region. A phenomenon within the Benguela Current. Inveatl. Rep. Div. Fish U n . S . Afr. No. 14, 36 pp.

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Corcoran, E. F. and Mahnken, C. V. W. (1969). Productivity of the Tropical Atlantic Ocean. Proo. Symp. Oceanogr. Fish. Trop. Atlant., Review papers and contributions Abidjan 1966 (UNESCO),57-68. Cromwell, T. (1958). Thermocline topography, horizontal currents and “ ridging ” in the eastern tropical Pacific. Bull. inter-Am. trop. Tuna Commn, 3, 136-164.

Curl, H. (1960). Primary production measurements in the north coastal waters of South America. Deep Sea RM.7, 183-189. Cushing, D. H. (1955). Production and a pelagic fishery. Fishery Invest., Lond. Ser. 2, 18 (7), 104 pp. Cushing, D. H. (1959). The seasonal variation in oceanic production as a problem in population dynamics. J . Cona. perm. int. Explor. Mer. 24 (3), 465-464. Cushing, D. H. (1961). On the failure of the Plymouth herring fishery. J . mar. b i d . A88. U K , 41 (3), 799-816. Cushing, D. H. (1962). An alternative method of estimating the critical depth. J . Colas. perm. int. Explor. Mer, 27 (2), 131-140. Cushing, D. H. (1963). Studies on a Calanzup patch. 2. The estimation of algal productive rates. J . mar. bwl. Ass. U.K., 43 (2), 339-347. Cushing, D. H. (in press). “ Food Chains in the Sea Oliver and Boyd, Edinburgh. Cushing, D. H. and Nicholson, H. F. (1963). Studies on a Cakanzup patch. 4. Nutrient salts off the north-east coast of England in the spring of 1964. J . mar. bi01. A88. U.K., 43 (2), 373-386. Darbyshire, M. (1963). Computed surface currents off the Cape of Good Hope. Deep Sea; Res. 10, 623-632. Darbyshire, M. (1967). The surface waters off the coast of Kerala, south-west India. Deep Sea Res. 14 (3), 296-320. Davies, D. H. (1968). The South African pilchard (Sardinopsooelkata).Preliminary report on the age composition of the commercial catches, 1950-56. InvestE Rep. Div. Fish Un. S . Afr. No. 33, 20 pp. Deacon, G. E. R. (1937). The hydrology of the Southern Ocean. “ Dieoovery ” Rep. 15, 1-124. Defant, A. (1936). Das Kaltwasserauftriebsgebiet vor des Kiiste Siidwestdrikas. Lmdesek. Forah., Munchen, 1936. 52-66. Emilsson, I. (1961). The shelf and coastal waters off southern Brazil. Bolm Ilast. Oceanogr. S. Paulo, 11 (2), 101-112. Fleminger, A. and Clutter, R. I. (1965). Avoidance of towed nets by zooplankton. fimnol. Oceanogr. 10, 96-104. Flores, L. A. (1967). Informe preliminm del crucero 6611 de la primavera de 1966 (Cab0 Blanco-Punta Coles). Infme Inst. Mar Per& No. 17, 16 pp. Flores, L. A. and Elias, L. A. P. (1967). Informe preliminar del crucero 6608-9 de invierno 1966 (Mancora-no). Infme Inat. Mar P d ,No. 16, 24 pp. Forsbergh, E. D. (1963). Some relationships of meteorological, hydrographic and biological variables in the Gulf of Panama. Bull. inter-Am. trop. Turn Cmmn, 7 ( l ) , 109 pp. Forsbergh, E. D. and Joseph, J. (1964). Biological production in the eastern Pacific Ocean. Bull. inter-Am. trop. Turn Commn, 8 (9), 479-527. Foxton, P. (1965). A mass fish mortality on the Somali coast. Deep Sea Res. 12

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( l ) , 17-19.

Frontier, 5. (1963). Zooplankton r6colt6 en mer d’kabie, Golfe Persique et h l f e d’Aden. Cah. O.R.B.T.O.M. O o h g r . 3,17-30.

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Fukuoka, J., Ballister, A. and Ccrgignon, F. (1964).An analysis of hydrographical conditions in tho Caribboan Sca (III)--ospccially about upwalling and sinking. Studies on Oceanography 1964, 145-149. Purncstin, J. (1959). Hydrologie du Maroc atlantiquc. Revue Trav.Inst. (scient. tech.) P&h. marit. 23 (l),5-77. Ganaparti, P. N. and Murthy, V. S. R. (1954). Salinity and temprraturc variations of thc surfaco wntcrs off tho Visalrhapntnam coast. Andhra Univ. Mem. Oceunogr. 1. 135-142. Garncr, D. M. (1961). Hydrology of Ncw Zcaland coastal waters, 1955. Bull. N . Z . Uep. acient. id. Rea. No. 138, 84 pp. Coldmnn, C. It. (1968). Tho use of absolutc activity for eliminating scrious crrors in tho mcnsiircmcnt of primary productivity with C“. J . Cona. perm. int. Explor. Mer, 32 (2),172-179. GuillOn, 0. C. and Flores, L. A. (1967). Informc prcliminar del cruccro 6702 dcl verano de 1967 (Cabo Blanco-Arica). Infme I m t . Mar Perti, No. 18, 17 PPGulland, J. A. (1968). Informe sobre la dinamica de la poblacion de anchoveta poruana. Dot. Inat. Mar Per&, 1 (6), 308-346. Gunther, E. R. (1936). A report on occanographical investigations in tho Peru coastal current. “ Discovery ” Rep. 13, 109-276. Hachey, H. B. (1936-37). Ekman’s theory applied to water replacemcnt on the Scotian Shelf. Proc. Trans.Nova Scotian Inst. Sci. 19 (3),264-276. Harden Joncs, F. R. (1968). “ Fish Migration”. Edward Arnold, London. Hart, T. J. and Currie, R. I. (1960). The Bcnguela Current. ‘‘ Discovery ” Rep. 31, 123-298. Harvey, H. W., Cooper, L. H. N., Lebour, M. V. and Russell, F. S. (1935). Plankton production and its control. J . mar. biol. Am. U.K.20, 407-441. Hayes, F. R. and Coffin, C. C. (1951). Radioactive phosphorus and exchange of lake nutrients. Endeavour, 10 (38),78-81. Hcinrich, A. K. (1961). Seasonal phenomena in plankton of the world ocean. 1. Seasonal phenomena in the plankton of high and low temperature latitudcs. Trudij Inst. Okeanol. 15, 57-81 (in Russian). Hentschel, E. (1933). Allgemeine Biologie des Sudatlantischen Ozeans. Erste Lieferung. Das Pelagial der obersten Wasserschicht. Wiss.Ergebn. d t . atlant. Exped. “Meteor”, 1925-27, 11 ( l ) , 168 pp. Hentschel, E.and Wattenberg, H. (1930). Plankton und Phosphat in dcr Oberflachcnschicht des Siidatlantischen Ozeans. Annln Hydrogr. Bed. 58, 273277. Hidaka, K. (1954). A contribution to the theory of upwelling and coastal currents. Trana. Am. geophys. Un. 35 (3),431-444. Hidaka, K. (1958). Computation of tho wind stresses ovcr tho Oceans. Rec. oceanogr. Wks Japan, 4 (2),77-123. Hidaka, K. and Ognwa, K. (1958). On tho seasonal variations of surfaco divcrgence of the ocean currents in terms of wind stresses over the oceans. Rec. oceanogr. Wks Japan, 4 (2),124-169. Holmes, R. W., Schaefcr, M. B. and Shimada, B. M. (1957). Primary production, chlorophyll and zooplankton volumes in thc tropical eastern Pacific Ocean. Bull. inter-Am. trop. Tuna Commn, 2 (4),129-169. Hutchinson, G. E. (1950). Survey of existing knowledgo of biogcochemistry. 3. Tho biogeochemistry of vertebrate excretion. Bull. Am. M u . nut. Hist. 96,654pp.

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Longard, J. R. and Banks, It. E. (1952). Wind-induccd vertical movement of the water on an opcn coast. T r a m . A m . Geophys. U n . 33 (3), 377-380. Longhurst, A. R. (1967). Tho pclagic phase of Pleuroncodee planipea Stimpson (Crustacca, Galathcidae) in the Californian Current. Rep. CalV. coop. ocean. Fish. Inveat. 11, 142-154. Lovegrove, T.(1962). The effect of various factors on dry weight valurs. Rapp. P . - v . Rdun. C o m . perm. int. Explor. Mer, 153, 86-91. Lynn, R. J. (1967). Seasonal variation of temperature and snlinity at 10 mcters in the California Current. Rep. Calif. coop. ocean. Fish. Invest. 11, 157-186. McAllister, C. D., Parsons, T. R. and Strickland, J. D. H. (1960). Primary productivity and fertility at station “ P ” in the north-east Pacific Ocean. J . Cons. perm. int. Explor. Mer, 25, 240-259. McEwen, G. F. (1929). A mathematical theory of the vertical distribution of temperature and salinity in water under the action of radiation, conduction, evaporation and mixing due t o the resulting convection. Bull. Scrippa Znam Oceanogr. tech. Ser. 2 (6), 197-306. McGowan, J. A. and Fraundorf, V. J. (1966). The relationship between size of net used and estimatcs of zooplankton diversity. Limnol. Oceanogr. 11, 456-469. McLaren, I. A. (1965). Some relationships between temperature and egg size, body sizc, development rate, and fecundity of the copepod PsewIocalanue. Limnol. Oceanogr. 10, 528-538. Marr, J. C. (1960). Tho causes of major variations in tho catch of the Pacific sardine Sardinop c a e d e a (Girard). I n Proceedings of the World Scientific Meeting on the Biology of Sardines and Related Species, held in Rome, 14-21 September, 1959. Vol. 3, pp. 667-791. FAO, Rome. Marshall, S. M. and Orr, A. P. (1955). ‘‘The Biology of a Marine Copepod, Calanua Jinmarchicw, (Gunnerus). ” Oliver and Boyd, Edinburgh. Matsumoto, W. M. (1966). Distribution and abundance of tuna larvao in the Pacific Occan. Proc. Governor’s Conf. on Central Pacific Fishery Resources. Honolulu, 1966 (T. A. Manar, Ed.), 221-230. Mazcika. P. A. (1967). Thermal domes in tho caatcrn tropical Atlantic Ocean. Limnol. Oceanogr. 12 (3), 537-539. Mensah, M. A. (1969). Zooplankton occurrence over the shelf of Ghana. Proc. Symp. Oceanogr. Fish. Trop. Atlant. Review papers and contributions. Abidjan, 1966 (UNESCO) 241-254. Mitchell-Innes, B. A. (1967). Primary production studies in the south-west Indian Occan 1961-63. I n m t . Rep. S. Afr. Ass. mar. b i d . Rea. 14. 20 pp. Nakamura, H. (1969). “ Tuna Distribution and Migration”. Fishing News (Books) Ltd.. 76 pp. Nathansohn, A. (1906). Uber die bedeutung vertikalrr WRsserl,ewegungen fur das Produktion des Planktons. Abh. Math-Phys. N a m e kilnigl. Sacha. Geaell. Wiss. 29. Nellen, W. (1969). Horizontal and vertical distribution of plankton production in the Gulf of Guinea and adjacent arcas from February to May 1964. Pmc. Symp. Oceanogr. Fish. Trop. Atlant. Review papers and contributions. Abidjan 1966, (UNESCO), 256263. Nielsen, E. S. (1952). The use of radio-active carbon (C14)for measuring organic production in the ma. J. Cone. perm. int. Explor. Mer, 18 (2), 117-140. Nielsen, E. S. (1964). On the determination of the activity in C14 ampoulcs. ICES CM 1964, Plankton Committee Doc. (106), 2 pp. (mimeo).

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Nielsen, E. S. and Hansen, V. Kr. (1959). Measurements with the carbon-14 technique of the respiration rates in natural populations of phytoplankton. Deep Sea Rea. 5, 222-233. .Nielsen, E. S. and Jensen, E. A. (1957-59). Primary oceanic production. The autotrophic production of organic matter in the oceans. Qalathea Rep. 1, 49-136. Orren, M. J. and Shannon, L. V. (1967). Letters to the Editors, Deep Sea Res. 14,279-280. Pavlov, V. Y . (1968). On the distribution of plankton in the vicinity of Cap Blanc. Okeanologiya, 8 (3),479-486. Posner, G. S. (1957). The Peru Current. Bull. Binghm oceanogr. Coll. 16 (21, 106-155. Rama Sastry, A. A. and Myrland, P. (1959). Distribution of temperature, salinity and density in the Arabian Sea along the south Malabar coast (South India) during the post-monsoon season.-Indian J . Fish. 6 (2),223255. Redfield, A. C. (1955). The hydrography of the Gulf of Venezuela. Papers in marine biology and oceanography. Deep Sea Rea. 3 (suppl.), 115-134. Reid, J. L., Jr. (1962a). Measurements of the California countercurrent at a depth of 250 metres. J . mar. Rea. 20 (2),134-137. Reid, J. L., Jr. (1962b). On circulation, phosphate-phosphoruscontent, and zooplankton volumes in the upper part of the Pacific Ocean. Limnol. Oceanogr. 7 (3),287-306. Reid, J. L., Jr., Roden, G. I. and Wyllie, J. G. (1958). Studies of the California Current system. Prog. Rap. Calif. wop. ocean. Fkh. Invest. 1966-58, 27-56. Richards, F. A. (1960). Some chemical and hydrographic observations along the north coast of South America. I. Cab0 Tres Puntaa to Curqao including the Cariaco Trench and the Gulf of Cariaco. Deep Sea Rea. 7 , 163-182. Riley, G. A. (1946). Factors controlling phytoplankton populations on Georges Bank. J . mar. Rea. 6 (l),54-73. Riley, G.A., Stommel, H. and Bumpus, D. F. (1949). Quantitative ecology of the plankton of the western North Atlantic. Bull. Binghm oceanogr. Coll. 12 (3),1-169. Rochford, D. J. (1962). Hydrology of the Indian Ocean. 2. The surface waters of the south-east Indian Ocean and Arafura Sea in the spring and summer. A w t . J . mar. Freahwat. Rea. 13 (3),226-251. Roden, G.I. (1961). On the wind-driven circulation in the Gulf of Tehuantepec and its effect upon surface temperatures. BeoJis. int. 1 (3),55-72. Russell, F. S. (1936). The seasonal abundance of the pelagic young of teleostean fishes in the Plymouth area. Part 3. T h e year 1935, with a note on the conditions as shown by the occurrence of plankton indicators. J . mar. biol. A88. U.K., 20, 595-604. Ryther, J. H., Hall, J. R., Pease, A. K., Bakum, A. and Jones, M. M. (1966), Primary organic production in relation to the chemistry and hydrography of the western Indian Ocean. Limnol. Oceanogr. 11, 371-380. Schaefer, M. B., Bishop, Y . M. N. and Howard, G. V. .(1958). Some aspects of upwelling in the Gulf of Panama. Bull. inter-Am. trop. Tuna Commn, 3 (2), 77-132. Schott, G. (1902). Die Auftriebzone an der Kuste von Sudwestafrika. WkS. Ergebn. dt Tiefeee-aped." Valdivia ", 1, 124-128.

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Adv. mar. Biol., Vol. 9, 1971, pp. 336509.

THE BIOLOGY OF WOOD-BORING TEREDlNlD MOLLUSCS N. BALAKRISHNAN NAIR The Marine Biological Laboratory, University of Kerala, Trivandrum 7 , Kerala, India and M . SARASWATHY Indian Ocean Biological Centre, National Institute of Oceanography, Cochin, India

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I. Introduction .. .. .. .. .. 336 .. .. 338 11. The Systematics and Distribution of the Teredinidae 111. Morphological and Anatomical Studies .. 344 , 390 IV. Thesexual Phases V. Fecundity .. .. 396 . .. . . 396 VI. Age or Size at Sexual Maturity . .. VII. Brecding Season .. .. 396 . VJII. Fert.ilization .. .. .. .. 399 . . .. .. 40 1 IX. Embryology and Larval Development A. The Gametes .. . . .. .. .. .. 40 1 B. Development .. .. .. .. . . .. .. 402 C. Duration of the Larval Period .. .. .. .. .. 406 D. Food of the Larvae . .. .. .. .. .. .. 407 E. Settlement . .. .. .. 407 X. The Season of Settlement .. .. 409 .. XI. The Pattern of Vertical Settlement 417 .. .. .. .. 424 XII. Teredinids in Deep Water .. X I I I . Growth Rates 425 XIV. Dispersal of Shipworms .. .. .. 428 xv. Physiological Studies .. .. 43 1 XVI. Food and Digestion . . . . .. 44 1 .. .. .. .. .. .. . . .. 446 XVII. Ecology A. The Influence of Temperature on the Activity and Distribution of Shipworms . .. .. .. .. 447 B. The Effects of Salinity 452 456 C. Occurrence in Fresh Water . . . . . . .. D. Illumination .. .. .. .. .. 457 E. Settlement in Relation t o Light and Gravity .. .. 467

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I. INTRODUCTION A ubiquitous pest of all manner of timber in the sea, t e r e d o t h e shipworm-causes damage worth millions of pounds every year all over the world. Hidden protectively within the ‘‘ heart ” of both fixed and floating timber, and hardly visible from the outside, these borers work silently and reduce t o soft sawdust even the most resistent timber. Rasping with their shells mechanically, these living drills draw a major part of their nourishment from the hard cellulose. Known to Pliny, Ovid and Aristophanes, shipworms are mentioned even by Homer. The accounts of the voyages of Dampier, Cook and Drake reveal that these early navigators dreaded shipworms. Columbus lost all the ships of his fourth voyage as a result of their ravages. Thus, unaware of the danger that lurked beneath them, ancient mariners were shipwrecked in mid-ocean through the rapacity of these wood borers. Even the safety of a nation was threatened owing to the ravages of the shipworms on the wooden dykes of Holland. Despite the care and constant surveillance of harbour engineers, teredo successfully invaded San Francisco Bay in about 1921. Unseen even by experts, this exotic menace converted solid pillars and piers into weak and fragile “ honeycombs ”. Along the entire seafront, bridges collapsed, piers crashed and boat hulls and wharf-piling crumbled. Like an unseen typhoon, it swept up the coast leaving a trail of destruction along its path. The first few waves of attack cost the United States several million dollars. I n a second serious outbreak in the same locality property worth 21 million dollars was destroyed. Though present in all seas, shipworms are particularly destructive in the tropical waters where they eat in-

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discriminately every material of plant origin. I n India alone millions of rupees are spent every year on the replacement of piles, jetties, fenders, boats, catamarans etc., destroyed by these organisms. Becker (1958) estimated that in India alone, the periodic cost of replacement of fishing craft destroyed by marine borers amounts to 2.5 million rupees. According to estimates by the U.S. Navy, the damage to boats, barges, bulkheads and other marine structures by borers in U.S. exceeds 60 million dollars every year. The destructive habits and biology of these molluscs have been the subject of much scientific interest and popular concern. Thcre is at the present time no comprehensive treatment of the biology of shipworms as a whole. The recent work of Turner (1966) provides a systematic compendium of the genera and species, yet many other aspects of study are treated only briefly. The absence of a comprehensive survey is surprising and is perhaps due to the fact that many papers are difficult to trace and many others, owing to their limited circulation, did not attract the attention they deserved. Knowledge of shipworms from parts of the world such as the Indian Ocean is particularly scanty and the morphological picture of even representative genera is far from satisfactory. The lack of information regarding many fundamental aspects is often surprising. Many accepted generalizations are invalid, the data on which they are based being of considerable age and unconfirmed or even incorrect. A critical survey of recent progress has not been easy, with no modern treatment of the group as a whole to serve as a basis for discussion. Students of invertebrate biology as well as those interested in problems of marine ecology are likely to benefit by a review of this kind. Such an attempt, while highlighting recent studies, will also indicate possible gaps in our knowledge of these pests despite the large number of published papers. What Korringa (1952) has so aptly said for oysters is equally true for shipworms. “. . . the greater the number of papers, the more we feel compelled to admit with complete candor and humility that we have but a poor understanding of many important factors in the oysters biology.” The scope of the present review is limited to papers dealing with the biology of shipworms. Papers concerning taxonomy have recently been adequately reviewed by Turner (1966) and are not emphasized here. Limiting this review to a few years only is likely to mar the fullness of the picture and so all relevant papers accessible to us have been included. The output of information on shipworms has been as erratic as their ravages which are “ periodically recurring devastations separated by often lengthy intervals of comparative freedom from attack.”

338

N. BALAKRISHNAN NAIR AND M. SUASWATHY

11. THE SYSTEMATICS AND DISTRI~UTION OF

THE

TEREDINIDAE

A perusal of the literature on teredinids will show that the taxonomy of this group has been in a state of utter confusion ; the description of one species could include several allied forms. The variations in taxonomical characters exhibited by individuals are so wide that exact determination of a species is extremely difficult. No other group seems to have a more unsatisfactory classification than the Teredinidae, as pointed out by several earlier authors. The reasons for this state of affairs have been : (1) many of the species included under this group have been created on the basis of fragmentary material, regardless of the wide range of variation exhibited by these bivalves ; (2) the locality of the type species has not been accurately determined; (3) many new species have been described on the basis of zoo-geographic provinces, without taking into serious consideration their means of dispersal ; (4) authors had described several new species without reference to all the earlier publications which were scattered and often unavailable. This has unfortunately resulted in the creation of many invalid species. While the taxonomy of the Teredinidae was in this state of confusion, Turner (1966) undertook the compilation of a comprehensive work to “ make available a catalogue of all the names used in the family Teredinidae; to illustrate as many of the type specimens as possible, giving descriptive notes concerning them, and to indicate synonyms whenever this could be done.” Turner had the rare opportunity, not available to many earlier taxonomists of this group, of examining many type specimens, an essential prerequisite for an attempt of this kind. Undoubtedly this work represents a milestone in the literature on the subject and will be an important work of reference for all future workers. Turner’s classification differs from that of earlier workers in that she has taken into consideration some features of the anatomy of the soft parts, and also the structure and manner of growth of the pallets, besides the conventional criteria for classification. Recognizing as many as fourteen genera, she discarded the usage of subgenera owing to the occurrence of transitional species between them. Turner divided the family Teredinidae into three subfamilies, namely Kuphinae Tryon, including the mud-boring genus Kuphw Guettard, Teredininae Rafinesque, w&h includes nine genera of shipworms, Bactronqhorua Tapparone-Canefri, Neoteredo Bartsch, Dicyathver Iredale, Teredothyra Bartsch, Teredora Bartsch, Uperotzcs Guettard, Psiloteredo

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T A BI.~ THEPATTERN OF DISTRIBUTION OF SHIPWORMS ALONG 81.

Andhra coast

Name of shipworm

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Madras coast

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1. 2. 3. 4. 5. 6. 7. 8. 9. 10. 11. 12. 13. 14. 15. 16. 17. 18. 19. 20. 21. 22. 23. IN -

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Bactronophorus thoracites (Gould) DicyathGer manni (Wright) Teredothyra srnithi (Bartsch) T . ezcawata (Jeffreys) . Teredora princesae (Siviokis) Uperotus rehderi (Nair) U . clawus (Gmelin) . Teredo furcifera Martens T .fulleri Clapp . T . clappi Bartsch . T . triangularis Edmondson Lyrodus a#nk (Deshayes) L. pedicellatus (Quatrefages) L. m s a (Lamy) Nototeredo e d m (Hedley). Nausitora dunlopei Wright N . h d l e y i Schepman Bankka bipenmta (Turton) B. bipdmulala (Lamarck) B. campanellata Moll/Roch B. c a r i W (Gray) B. nwdiMoll B. rochi Moll

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THE

COASTSOF INDIA

Andamans

Bombay

340

N. BALAKRISHNAN

NAIR AND M. SARASWATRY

Bartsch, Teredo Linnaeus and Lyrodus Gould, and the new subfamily Bankiinae which includes four genera-Nototeredo Bartsch, Xpathoteredo Moll, Nausitora Wright and Bankia Gray. According to this new system the total number of valid species in the world has been reduced to 66. This is bound to be of considerable help to all teredine workers and will enable even relatively inexperienced persons to determine the forms before them with a fair amount of accuracy. Also, this revision has brought together a great deal of the scattered earlier literature in the form of illustrations and descriptions of the several species along with ways and means of determining them. Turner has synonymized several species. There has been undue splitting of species in this group because of incorrect identification owing to the non-availability of representative series of well preserved specimens for accurate specific determination. With this new classification as a basis, we investigated the pattern of distribution of shipworms along the coasts of India and also the nature of their occurrence in the Indo-West Pacific. This should be of interest since information on this is far from complete. I n Table I is presented the pattern of distribution of shipworms along the Indian coasts. This is by no means an exhaustive list because studies on the incidence and activity of marine borers have been undertaken only in selected areas along the east and west coasts of India. While 23 species are active along the east coast, only about 10 have been recorded from the west coast and all these occur along the east coast as well. Of these Dicyathifer manni, Teredo furcifera, Bankia campanellata and Bankia carinata are present in almost all areas from which records are available. Bactronophorus thoracites, Teredo princesue, Teredo clappi, Nausitora hedleyi and Bankia rochi occur on the east and west coats of India but have not been collected from all the regions. At least 6 species of shipworms occur in West Bengal. From the mangrove swamp forests of the Sunderbans, Bactronophorus thoracites has been reported as a serious pest infesting both living and dead trees, weakening them so that they break off before strong winds (Roonwal, 1954, 1954a). Nausitora dunlopei, Bankia rochi, B. campanellata, B. carinata and B. nordi are the other 5 species reported as active in West Bengal (Roch, 1955 Rajagopalaiengar, 1961, 1964). No systematic work on these borers has been undertaken around Calcutta and information is limited regarding the exact number of species that occur and their biology. Nausitora dunlopei is a very interesting species reported in timbers exposed to almost fresh water in the river Comer, a tributary of the Ganges, 150 miles up river (Wright, 1864). The ability of the species to live in almost fresh water is of special interest. The marine wood-borers of the Andhra coast have been studied by

THE BIOLOGY OB WOOD-BORING TEREDINID MOLLUSCS

341

Nagabhushanam (1958, 1960), Ganapati and Lakshmana Rao (1959). No less than 13 species of shipworms seem to exist in that region, Bankia campanellata and Teredo furcifera being by far the most important from the standpoint of destruction at Visakhapatanam Harbour. Along the Madras coast 20 species are apparently active of which only 4 occur in any abundance (Nair, 1954, 1955, 1956b). The most important forms infesting the fishing floats are Bankia carinata and Teredora princesae and along the coast Teredo furcifera and Uperotus rekderi are destructive. Uperotw clavus infests the floating seeds of the mangrove and these are cast ashore in large numbers during the monsoons (Gravely, 1941 ; Nair, 1954). Nearly seven species are active in and around Bombay (Palekar, 1956; Palekar and Bal, 1955, 1957, 1957a, Becker, 1958). The dominant forms here are different from those in other localities. According to recent reports most of the destruction is caused by Dicydhifer manni, Bankia rochi and also by Teredo furcqera. Only 8 species of shipworms have so far been collected from the south-west coast of India. In the environs of Cochin Harbour, a typical tropical estuary, the most destructive species are Nausitora hedleyi and Teredo furcifera (Nair, 1965, 1966). There is thus a marked difference in the occurrence and distribution of species along the east and west coasts of India. Recently Panikkar (1969) has tried to explain the differences in the nature and composition of the fauna of these coasts. According to Panikkar, " the estuarine, and to some extent, the shore fauna of the west coast of India, suffers from partial or complete destruction during the South West monsoon period and that this is followed by an annual repopulation of the estuaries and backwaters after the monsoon months. With the cessation of the rainy season when heavy run-over of fresh water to the sea takes place, more stable conditions prevail in later months in the estuaries which slowly build up a saline regime." The occurrence, abundance and activity of the borers show remarkable variations and fluctuations in the different harbours of India, each having its own dominant set of species and an assemblage of less important forms. It is well known that reactions of closely allied species may be different and even individuals of the same species may vary according to the peculiar hydrographic conditions prevailing in an area. It is noteworthy that each species has its characteristic preferences, distinctive life history and seasons of settlement. Generalizations should therefore be made with great caution and a scheme evolved after elaborate study and experimentation for one locality may prove in-

342

N. BALAKRISHNAN NAIFi AND M. SARASWATHY

applicable for another. Species density has fluctuated over long periods and within the same period their attacks have differed considerably in various locations along the same stretch of coast (Becker, 1958). So the problem varies with the species occurring in any locality and also with climatic and hydrographic conditions. The vagaries and discriminations of these pests are such that most of the conclusions drawn from any investigation must usually be considered as purely of local application and the experience gained from one locality cannot necessarily be applied to another. Each harbour or geographical location needs a special set of specifications for the treatment of timber owing to the difference in the species of borers prevalent, the condition of the water, degree of pollution, etc. Table I1 gives the distribution of shipworms in'the Indian Ocean. According to revised estimates nearly 35 species occur. So as to present the nature of their distribution, the land masses bounding the Indian Ocean have been tentatively divided into four regions: Region I, East Coast of Africa, Madagascar, Red Sea and Persian Gulf; Region 11, India and Indian Ocean Islands; Region 111, Burma, Malaysia and Indonesia ; Region IV, Australia and New Zealand. It is evident from the table that even though species are not uniformly distributed, the records of certain species do indicate wide distribution extending from the East Coast of Africa to Australia and New Zealand. The 35 species noted from the area may be grouped into nine categories, on the basis of this distribution. (1) Species which have been recorded from all the four regions: Dicyathifer manni, Uperotus clavus, Lyrodus pedicellatus, Nausitora dunlopei . (2) Species common for Regions I , I1 and I11 but not recorded from Region IV: Teredora princesae, Teredofurcifera, T .fulleri, T . clappi, Lyrodus massa, Bankia rochi, B . bipalmulata. (3) Species which are common for Regions 11, I11 and I V : Bactronophorus thoracites, Nototeredo edax. (4) Species which are common for Regions I and I1 only: Teredothyra smithi . ( 5 ) Species common for Regions I1 and I11 only: Lyrodus aflinis, Nausitora hedleyi, Bankia campanellata, B . carinata. ( 6 ) Species which are common for Regions I11 and IV only : Teredo navaliis. ( 7 ) Species which occur in Regions I and I11 only : Teredothyra matocotana, Spathoteredo obtusa.

THE BIOLOGY OF WOOD-BORING TEREDWZD MOLLUSCS

343

TABLE11. THENATURE OF DISTRIBUTION OF SHIPWORMS IN THE INDIAN OCEAN Region I

Name of specim

Region 11

Region 111

+

+ + + + + + + + + + -

Region I V

, -

1. Bactronophorus thoracites (Go Neoteredo reynei (Bartsch) 3. Dicyathifer manni (Wright) . 4. Teredothyra smithi (Bartsch) 5. T . excawata (Jeffreys) 6. T.matocotana (Bartsch) . 7. Teredora princesae (Sivickis) 8. Uperotw rehderi (Nair) . 9. U . chwus (Gmelin) 10. Teredo furcifeera Martens 11. T . fuller; Clapp 12. T . ckappi Bartsch 13. T.triangularis Edmondson 14. T . bartach4 Clapp . 15. T . somersi Clapp . 16. T . navalis Linnaeus . 17. T.mindanensis Bartsch . IS. T. johnsoni (Clapp) . 19. Lyrodw aflnis (Deshayes) 20. L. pedicellatus (Quatrefages) 21. L. mmsa (Lamy) 22. Nototeredo edax (Hedley) 23. Xpathoteredo obtwa (Sivickis) 24. NauBitora dunlopei Wright 2s. N . hedleyi Schepman . 26. Bank& bipenrutta (Turton) . 27. B. campanellata Moll/Roch 28. B. carinata (Gray) 29. B. nordi Moll 30. B. rochi Moll . 31. B. m r t e n s i (Stempell) 32. B. awtralis (Calman) 1. B. orcutti Bartsch 34. B. gracilis Moll . 35. B. bipalmulaia (Lamarck) 2.

.

.

-

.

+ + + + + + + -

.

.

.

.

. .

.

. . .

+ + + -

-

+ + + + + + + + ++ +

.

Region I: Region 11: Region 111: Region IV:

+ + + + + + + + + + + + + + + +

.

+ present;

-

- not recorded.

East coast of Africa, Madagascar, Red Sea and Persian Gulf. India and Indian Ocean Islands. Burma, Malaysia and Indonesia. Australia and New Zealand.

344

N.

BALAKRISHNAN NAIR AND M. SARASWATNY

(8) Species which are common for Regions I and I V but not recorded from I1 and I11: Teredo bartschi. (9) Species which give no evidence of a particular pattern of distribution : Neoteredo reynei, Teredothyra excavata, Uperotus rehderi, Teredo triangularis, T . somersi, T . mindanensis, T .johnsoni, Bankia bipennata, B. nordi, B. martensi, B. australis, B . orcutti, B. gracilis.

The distribution of shipworms in the Indian, Pacific and Atlantic Oceans, including the Mediterranean is presented in Table 111. It is evident that there is a preponderance of shipworms in the Indo-West Pacific region with more than 40 out of the 66 known species occurring there. Three species-Lyrodus pedicellatus, Bankia carinata and Teredo bartschi-are noteworthy in that they show a very wide distribution, having been recorded from all these areas. Six species are common to the Indian, Pacific and Atlantic Oceans while 16 species occur both in the Indian and the West Pacific. Two species are common to the Atlantic and the Mediterranean (Teredora molleolus, Nototeredo norvagica), 3 to the Pacific and Atlantic (Lyrodus takanoshimensis, Bankia jimbriatula, B. gouldi) and 1 to the Indian and Atlantic Oceans (Bankia campanellata). The distribution of some species is restricted to certain oceans. For example, 8 species, Uperotus rehderi, Teredo aegypos, T . poculifer, T . somersi, Bankia anechoensis, B. australis, B. brevis and B. nordi occur only in the Indian Ocean; 13 species, Kuphus polythalamia, Teredo mindanensis, Lyrodus m s s a , L. mediolobata, Nausitora dryas, N . excolpa, Bankia barthelowi, B. cieba, B. fosteri, B. orcutti, B. philippinensis, B. setacea and B. zeteki have so far been reported only from the Pacific Ocean, 4 species, Uperotus panamensis (?), Psiloteredo senegalensis, P. megotara, Nototeredo knoxi, from the Atlantic only, and 6 species, Teredothyra dominicensis, Psiloteredo healdi, Teredo johnsoni, T . portoricensis, Spathoteredo spathu and Bankia destructa, from the Gulf of Mexico and the Caribbean only. The distribution of 4 species, Neoteredo reynei, Uperotus lieberkindi and Lyrodus bipartita and Bankia gracilis, is doubtful, probably because they were collected from drift material.

111. MORPHOLOGICAL AND ANATOMICAL STUDIES A survey of the morphology and anatomy of shipworms is an essential prerequisite for (1) a clear understanding of the relationship of the different species and genera and (2) for a proper assessment of the nature of the specialization within these bivalves which have resorted to a unique diet on wood-a terrestrial product. Consequent on

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345

the observation of Turner (1966) that the characters of the organ systems, as well as of the shell and pallets may be used in taxonomy and phylogeny, there is imperative need for more accurate information about the morphology and anatomy of as many species as possible. The morphological studies of Sellius (1733) and Adanson (1765) established the taxonomic status of these long, cylindrical and almost naked bivalves and cleared the confusion regarding their position among invertebrates. One of the most notable studies on the anatomy of shipworms is that of Sigerfoos (1908) who worked on Bankia gouldi. Earlier workers like Deshayes (1848) and Quatrefages (1849), studied teredine anatomy but the exact identity of the species they worked on is doubtful. Subsequent to the work of Sigerfoos, Nair (1955, 1957a, 1964) investigated in detail the anatomy of Bankia indica (=B. carinata according to Dr Ruth Turner). Potts (1923) described the structure and function of the " liver ') of Teredo. Lazier (1924) gave an account of the morphology of the digestive tract of Teredo navalis. Yonge (1926) examined the detailed structure and suggested the function of the digestive diverticula of Teredo along with other lamellibranchs. A general account of the anatomy of certain organ systems of Bankia (Bankielkz) minima has been published by Bade et al. (1961, 1963-64). The most comprehensive work undertaken so far on the gross morphology of representative species of the Teredinidae is undoubtedly that of Turner (1966) who undertook an elaborate survey of the gross structure of several species for taxonomic purposes. This work was based on dissections of the animal. No sectioning or histological studies were attempted owing to absence of suitably preserved materjal. Thus information about the general anatomy of the genus Bankia is fairly complete through detailed studies on 2 species. There is some information about the anatomy, especially of certain organ systems of the genus Teredo (Potts, 1923; Lazier, 1924; Yonge, 1926; Miller, 1922, 1923, 1924; Coe, 1933, 1934, 1936; Grave and Smith, 1936; Coe, 1941; Purchon, 1941; Grave, 1942; Coe, 1943; Lane, 1959; Bade et al., 1961, 1963-64). Recently Saraswathy (1967) made detailed studies of the structure of Nausitora hedleyi Schepman, Teredo fwrcifera Martens and Teredora princesae (Sivikis). Unlike other bivalves, shipworms have a soft, vermiform body (Fig. 1) which gives them a resemblance to worms. They are highly specialized bivalves, adapted for boring into wood and the bivalve shell has lost its protective function and become an effective drilling tool. Despite their unique appearance their close relatives are the piddocks with which they are grouped under the sub-family Pholadinae

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

dfrica, West coast

wediterraman

Europe, Atlantic coast

7reenland

East of North America and

?ulf of Mexico and Caribbean

gouth America, East Coast

gouth America, West Coast

Tentrat America, West Coast

West coast of North America

Yawaiian Islands Widway Island8

Vorth-western Pacific

Tapan

Philippine Islands

Pacific Islands S.E.Asia, mndomwia, New Guinea

4wrtralia and NEWZealand

India, Indian Ocean Islands

Vast coast of Africa, Madagascar, Red Sea, Persian Gulf

20. g-. ,,m-.Alipr

In.rlnl

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