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.

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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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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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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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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.

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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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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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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 . ..

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.. The Systematics and Distribution of the Teredinidae . .

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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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IV. The Sexual Phases V. Fecundity

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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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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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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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XXI. Acknowledgements XXII.

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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

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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

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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

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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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(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

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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

THE BIOLOGY OF ASCIDIANS

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

THE BIOLOGY OF ASCIDIANS

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

THE BIOLOGY OF ASCIDIANS

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

<6OC

(1

Notknown

(6°C

of Norway of Norway

ca. 100 m 0 to 5 m

6 to 9°C

- 1to 20°C

<1 2

6 to 18°C 8 to 23°C

of Sweden of Sweden

15 to 30 m 0 to 10 m

- 1 to 18°C

5 t o 15°C

1 2

Not known May-June Aug.-Sept June(-July) MayJune (July-)Aug.Sept. Autumn Spring (Summer) Greater part of the year

Sub-Arctic

KJ

RELATIONSHIP TO TEMPERATURE OF Ciona inteatinalia f. typica

Depth

Region

West coast West coast in poller West coast West coast

THE

South coast of England (Plymouth)

Surface water

6 to 16°C

2(to 3)

French Mediterranean coast

Surface water

10 to 26°C

At least 3

Gulf of Naples

Surface water

13 to 27°C

At least 3

Sub-tropical and tropical

Surface water

20 to 32°C

3 to 4 or

more

I+

Temperature tolerance range Larvae Adults

Zygote4

8 to 22OC 8 to 22OC

8 to 23°C (at any rate in winter) The whole 14 to 27°C year (in winter upper limit is possibly at 23 to 24°C) Not known Upper limit is probably sometimes above 30°C (e.g. at Suez)

0 to 21°C (on Murmansk coast)

- 1 to 30°C 6 to 24°C-1 to ca. 30°C 6 to 24°C - 1to 08.30"C

8 t o 40°C

'

THE BIOLOGY OF ASCIDIAN’S

26

out the geographical range of the species, but as a rule two generations live side by side for much of the time. Comparisons drawn from populations living in widely separated regions are suspect because of the possible existence of physiological races (Runnstram, 1927, 1929, 1936), although Dybern doubts the evidence for these. The effect of temperature is clearly shown, however, by a comparison of the growth and annual cycle of C. intestinalis in two British docks, one of which was subject to heating by a power station (Millar, 1952; Naylor, 1965a, 1965b) (Fig. 10). In a single population, too, the growth rate rises with the temperature, and Sentz-Braconnot (1966)found that Ciona settling in the early part of the summer reached Jan

Feb Mar *Pr

May 0

1 I

90

Jun

@

0 V

Ju 1

d

Aue

SeP

-

Oct

Nov

40 20

Dec

0

2

4

6

E

l

0

Body length, cm FIQ.10. Effect of temperature on growth and annual cycle in Ciona inleatidia ; A, in a dock at Ardrossen, Scotland, and B, in a heated dock at Swansee, Wales (redrawn from Neylor, 1966b).

26

R. H. MlLLAR

only 1-3 cm in 45 days, but later in the summer grew to 4-5 cm in the same time. Similarly, Corella willmerianu in coastal waters of Washington, U.S.A., completes its life in 5 months if it settles in time to grow rapidly during summer but takes 7-8 months if growing more slowly in winter (Lambert, 1968).Under favourable conditions, growth to sexual maturity is rapid, and specimens of Molgula manhattensis only three weeks old can release eggs (Grave, 1933). Faster growth, earlier death, and a quicker succession of generations appear to be characteristic of life in warm water and, in the almost total absence of information on available food, temperature is justifiably regarded as of priinc importance. In British waters Cionu lives for 12-18 months (Orton, 1914, 1920; Millar, 1952),but in the tropics for only a few months and in sub-Arctic waters probably for a few years (Dybern, 1965). Curiously enough it is known to survive for two or more years at Marseilles (PkrAs, 1946) and at Millport, Scotland, young specimens brought in from the sea lived in the aquarium t o an age of about 38 years (personal unpublished record). Other solitary ascidians have been less studied but appear t o have similar life cycles. Ascidiella aspersa (Miiller)lives for 12-18 months in British waters (Millar, 1952; Gage, 1966), but on the Norwegian coast its life varies from one to three years, according t o water temperature (Dybern, 1969a). Corella parallelogramma is also essentially an annual, but Ascidia mentula Muller may live for at least three years (Dybern, 1969a). Millar (1954b) found that Dendrodoa grossuluria has a life span of 18-24 months on British coasts, and that three generations arc simultaneously present in the population. The maximum age of Styela coriacea is about 20 months, and three or four generations are produced annually (Diehl, 1957). In only a few species does the animal bear any clear evidence of its age, but in the genus Chelyosoma the test is divided into a number of hard plates with concentric lines (Fig. 11). These apparently represent

Fro. 11. Cklyosorno rnacleayanvrn ; dorsal view of e specimen in its fourth year, showing plates with growth lines (redrawn from Huntsman, 1921).

THE BIOLOGY OF ASCIDIANS

27

winter growth checks, and Huntsman (1921) found that C . macleayanum Broderip and Sowerby continues t o grow for more than four years in Alaskan waters, C . productum Stimpson for more than three years and G. columbianum Huntsman for only one year. Although species with a wide latitudinal range show great variation in tho life cyclc, which can be compressed into a few months in the warni part of tlic range, warm-water species of restricted distribution tnny not havc such a rapid tuni-over of generations or such a short life. Thus Ascidia nigra in Jamaica attains an age of 18-22 months (Goodbody, 1962). Styela plicata (Lesueur), a warni-water species of rather wide distribution, appears t o live for 5-6 months in warm years and 7-8 months in cold years (Kanatani et al., 1964). Est,imates of the life span of a species do not, of course, imply that t he whole population dies more or less simultaneously, although catmast,ropliicniortalitics have been recorded, as in three species in ,Jamaica which were decimated by a sudden influx of fresh water following heavy rain (Goodbody, 196lc). Sudden high mortalities are soinctimcs due to the death of the organisms on which the ascidians liavc scttlcd, McDougall (1943) having noted cases of the rapid disappearance of Styela plicata and Atlolgula manhuttensis when their supporting Bugula and Tubularia died. Amongst other causes of mass niortality is low winter temperature, and the fate of Ciona intestinalis, Jlolgula inanhattensis and Styela plicata, in the lagoon of Venice is incntionccl clscwhere (Sabbadin, 1957). In the absence of such dramatic events, much of the mortality can be ascribed to the activity of predators and competitors, and ultimately to t'lic onset-of senescence (Goodbody, 1962). Goodbody (1961a, 1963a) was able to follow the course of events in populations of Ascidia nigra. During the six wccks after settlement 97-08% of the young ascidians usiiiilly died, with ext.rcmes of lOOyoand 82.5%. The different survival rii.t,cs iirc related t.0 differences in the associated plant and animal c~otnriiuiiit,ics,sonic members of which may have competed with the young :iscidi;ins or physically displaced them. After this critical cwly period the prcssurcs appear to be much less, and the individuals which survive it have a good chance of completing their potential lifespan. Kot undil 18-22 months after settlemcnt is there another sharp tlrcliiie in nuinbers, and a t this t>imethe animals probably die of old age (Fig. 12). In cornpound forins, as already noted, thc existence of a colony with it,s niiiny zooitls undergoing t'hcir own cycles of growth, budding and rcgenen~t~ion, ninkes the assessment of growth more difficult than in the solitary f o r m . The simplest approach relies on successive measure-

28

R. H. MILLAR

50

De ys FIG. 12. Aacidia nigra. Survival curve for three groups, appearing on test panels in August (.--.), September (-------)and October (..........) (redrawnfrom Goodbody 1962).

ments of the areas of colonies in a population (Millar, 1952). Although this method may be satisfactory in the botryllids, in which colonies in nature generally remain intact and discrete, the work of Oka (1942) and

10

20

30

Days

FIQ.13. Polycilor mufabilis. Growth of a group of colonies derived by division of one parent colony. The total area of the daughter colonies is plotted on a logarithmic scale, against time (redrawn from Oka and Usui, 1944).

THE BIOLOGY OF ASOIDIANS

29

Oka and Usui (1944) showed that colonies of Polycitor mutabilis Oka divide repeatedly. Division takes place both by simple fission, and by colonial budding in which zooids extruded from the parent colony give rise to new colonies. Moreover, colonies of this species undergo cyclical expansion and contraction. By considering all the daughter colonies derived from one original colony as a composite unit Oka and Usui were able to show that the area plotted on a logarithmic scale bears a linear relationship to time (Fig. 13). Division of the colony also occurs in Didemnum candidum Savigny (Carlisle, 1961) and Archidistoma aggregatum Garstang (Nakauchi, 1966a), and here, too, the area of all the daughter colonies would have to be used in growth studies. Sabbadin (1960) measured the growth of Botryllus schlosseri, not by the area of colonies, but by the number of zooids, and found this to vary so widely that in the fifteenth generation of blastozooids different colonies contained between 1 and 97 zooids. Growth is further complicated by periodic rejuvenescence, with parts of the colony proliferating while other parts degenerate. Earlier, it had been shown for the same species that the zooids may double in number every two or three days and that a fast-growing colony attains 1 000-2 000 zooids within a month of its establishment (Grave, 1933). Growth may be interrupted and later resumed, and Nakauchi ( 1966b) observed that colonies of Aplidium multiplicatum (Sluiter) increased in size until, at a temperature of about 3OoC, breeding took place. At this time growth of the colony ceased, and the zooids regressed and divided ; only later, when the sea temperature had fallen to 25OC did the buds develop into new zooids. Then active life and growth of the colonies were resumed, followed by further breeding. It is not clear whether interruption of growth was associated primarily with breeding or with the high temperature. The involved questions of the physiological control and mechanics of budding are beyond the scope of this review and have been discussed by Berrill (1951), but it may be stated that in general " the phases of maximum sexual and asexual reproduction alternate " (Berrill, 1935b), with the sexual process confined to summer. After the breeding season the zooids usually undergo a process of budding and the colonies may pass the winter in a relatively inactive condition, in some cases being reduced to masses of dormant buds. Temperature affects the balance between regression of zooids and subsequent differentiation into new zooids, as Barth and Barth (1966) showed in Perophora viridis Verrill. It appears, however, that in some species low temperature merely retards recovery of the colony, and Vernay (1955) found that the buds of Synoicum argue slowly develop into functional zooids throughout the

30

It. H. ItULLAR

winter. Similarly Archidistoma aggregatum and Diazona violaeea Savigny develop during the winter (Berrill, 1948b, 1948~).In functional colonies of Metandrocarpa taylori Huntsman asexual reproduction takes place throughout the year (Abbott, 1953), but is least intensive when breeding is in progress, in the summer (Haven, 1967). Sabbadin (1955) recorded budding in Botryllus schlosseri at all seasons, although the process was slower in winter. Naukauchi (1966a) considered that budding is of two functional types. One of these involves resorption of the zooid, is an adaptation to adverse conditions, and may take the form of hibernation (Clavelina, Diazona, Syndiazona, Perophora) or aestivation (Aplidium multiplicatum) ; the other, which is not accompanied by resorption of the zooid, occurs in favourable conditions and results in growth of the colony (Perophora, botryllids, polycitorines and some polyclinids). The alternation of the sexual and asexual process in compound ascidians is therefore a complex pattern of events, further complicated by the fact that in some genera all buds can reproduce both sexually and asexually whilst in others different sets of buds are restricted to one method (Ivanova-Kazas, 1967). A few compound ascidians, in which the colony is very distinctly divided into stalk and head, show particularly clearly a cyclic degeneration and regeneration. Sycozoa sigillinoides Lesson has a long, narrow, sometimes branched stalk surmounted by heads containing the functional zooids. Following breeding, the heads disintegrate or break off, leaving headless stalks containing buds derived from the vascular processes of zooids (Caullery, 1909; Salfi, 1925) (Fig. 14). In this reduced state the stalks recall the overwintering condition of certain species of Polyclinidae. The stalks of Sywzoa subsequently grow new heads, when the buds develop into zooids which secrete fresh test material (Millar, 1960). It would be interesting to know whether the whole process is repeated year after year. In the related genus Hgpsistozoa, one of the most highly evolved of all compound ascidians, having a very complex embryonic and larval development (Brewin, 1956a),the colony is also divided into a stalk and head, and, as in Sycozoa, breeding is followed by dissolution of the head which is later replaced through the activity of zooids at the top of the stalk. Hypsistozoa illustrates the alternation of sexual and asexual processes (Fig. 15), and it is interesting to note that budding and growth of the colony occur in summer and autumn whereas sexual reproduction is confined to the winter and spring, thus reversing the more usual seasonal sequence. A plentiful supply of plankton is available during gonad maturation and embryological development (Brewin, 1956a), and may be particularly im-

THE BIOLOGY OF ASCIDIANS

31

a

1 FIO.14. Sycozon aigillinoidee. Colonies. a, with stalk and fully developed heads; b, with hoadlcss stalks; c, with new heads developing from an old stalk.

portant since the parent zooids nourish the embryos for several months . Colonies not only may divide, but in some species may fuse. Bancroft (1903) found in Botryllus sp. and Botrylloides sp. that unrelated colonies would not fuse, but that closely related colonies might do so. Further investigations by Oka and Watanabe (1957, 1960) and by Mukai (1967) revealed something of the genetic basis of the phenomenon but the extent t o which fusion occurs in nature remains uncertain. The life-span, like the growth-rate, is more difficult t o determine in compound than in simple ascidians, because of their periodic reduction and regeneration. There may even be grounds for regarding the colony of some species as potentially immortal (Sabbadin, 1960). I n the field it is difficult t o identify and follow the fate of individual colonies, and

32

R . H. ‘MTT.T.bR

FIQ.16. HypGtozoa jaameriana. Annual cycle of sexual and asexual reproduction (redrawn from Brewin, 1966af.

laboratory studies raise doubts about how far the observed events correspond to those taking place in nature. A few observations indicate the longevity of certain species (Table 11). The causes of death in compound forms, other than by the activity of predators (see p. 48) are little known, but presumably are similar to those applying to simple ascidians. Intraspecific competition may sometimes eliminate the less vigorous specimens, according to Bancroft (1903), who also noted that colonies of Botryllus lost vigour and shrank before dying, apparently from old age. A further cause of death, which affects compound and solitary forms dike, is detachment from the substratum, when the animals may drift away to unsuitable conditions or be cast ashore. Schwartz et al. (1960) studied Aplidium cowtellatum (Verrill)in Sinepuxent and Chincoteague Bays, which are shallow landlocked areas on the east coast of the U.S.A. Specimens were common but unevenly distributed, and in the more

33

THE BIOLOGY OF ASCIDIANS

TABLE11. LIFE-SPAN OF SOME COMPOUNDASCIDIANS Clavelinu picta C . oblonga Hyp8iatozoa faameriuna Perophota bermdensis D i p l o e m lblerianum Diazona violacea Bott$h sch~oeseri

Botrylloidea leachi

at least 3 years 13 years at least 24 years 1-2 years 1-1+ years 4-5 years under 1 year 1- 1 years 12-20 months at least 2 years

+

Berrill, 1932 Berrill, 1932 Brewin, 1959 Berrill, 1935b Millar, 1952 Berrill, 194% Bancroft, 1903 Millar, 1952 Sabbadin, 1955 Dybern, 1969s

sandy parts many were moved by wave action, resulting in heavy mortalities amongst populations established on unstable bottoms.

V. ECOLOGY A. The numbers and biomass of mcidians The part played by ascidians in the economy of the sea is poorly understood, and only recently has quantitative information started to accumulate. Certainly in some kinds of habitat they are of little importance (Picard, 1965), but elsewhere are sufficiently numerous to merit attention. Their place in fouling communities-often a dominant one-has been mentioned, and the instance noted by Elroi and Komarovsky (1961) of a wet weight of Ciona intestinulis amounting to many kg/m2 illustrates the importance of the group in certain circumstances. In natural communities, too, ascidians are sometimes amongst the dominant groups, as Abbott (1966) found in an area surveyed near Cape Thompson, Alaska. The most striking examples of dominant ascidian species are to be found amongst the family Pyuridaa. On parts of the coast of New Zealand, rocks may be covered by a single species (Oliver, 1923), and the Pyura-zone is also one of the most characteristic features of the intertidal rocks of the coast of New South Wales, Australia, where Pyura praeputialis (Heller), a species occurring along 1 000 miles of coast, covers a band 2 f t in width (Dakin et al., 1948). The related Pyura stolonifera (Heller) occupies the same ecological niche on South African shores, sometimes over a vertical zone of 34 f t (Morgans, 1959), and Pyura chilensis Molina, a species of similar habit, forms a dense cover on rocky shores in Chile (Gutihez and Lay, 1965). Sheltered shores, too, may provide very favourable conditions, and Lewis and Powell (1960) found Ascidiella aspersa and C i o m intestidis to be dominant over all other animal species on parts of the Scottish coast.

34

R. H. MILLAIt

In sublittoral arcas species of the family Molgulidae are sometimes strikingly prolific, and Dragovich and Kelly (1964) found molgulids to be the most numerous organisms in trawlcd samples in Tampa Bay, Florida. Abbott (1951) recorded a mass of Bostrichobranchus digonas Abbott cast up on a Florida beach and forming a belt 4-6 in wide and about 100yd long, indicating the abundance of the species in an adjacent sublittoral arca. And at Point Barrow, Alaska one short haul brought up a dredge one third filled with thc molgulid Rhizomolgula globularis (Pallas), and containing little else (MacGinitie, 1955). Large areas of the bottom in the shallow inshore parts of the Gulf of Naples are " literally covered " with Ascidiella aspersa, which is there the dominant animal (Parenzan, 1959), and in the harbour of Genoa ascidians are abundant with C i o m intestinulis a very important species in the quantitative composition of the sessile benthos (Relini, 1962). The frequent descriptions of escidians as " abundant " or " in great numbers " testify to the significant role which they must play in many parts of the sea. Nevertheless, rather few measurements have been madc of their abundance. Quantitative studies of the sublittoral fauna are more easily made on soft than on hard substrata, and most of the data have resulted from the use of grabs applied to sandy and muddy areas. A benthic survey of Scottish and adjacent waters indicated maximum ascidian densities in some places of about 100 per m2for Eugyra arenosa (Alder and Hancock) and Polycarpa Jibrosa (Stimpson) and of nearly 200 per m2for Pelonaia corrugata Forbes and Goodsir (Thompson, 1930 ; 1931 ; 1932 ; 1934). During an investigation of the fauna of brackish ponds in Japan, Kikuchi (1964) estimated the biomass of different animal groups and the figures show that ascidians could constitute about an eighth of the total benthic crop. Somewhat similar figures were obtained by Pdrhs (1967) for a typical coastal detritus fauna in the Mediterranean, where ascidians accounted for 11.5y0, 10.Syo and 0% of the total dry weight of the bottom fauna a t three stations, although in numbers of specimens they represented only 0.7%) 2.6% and 0% respectively. At two stations on a muddy detritus bottom 60.3% and 19.3% of the total fauna by dry weight were ascidians and 5.3% and 2.2% of the total number of specimens. The discrepancy between estimates of importance using dry weight and numbers is, of course, explained by the relatively large size of the ascidians compared t o that of other animals. Sanders (1960) listed 76 species in a soft-bottom community in Buzzards Bay, U.S.A., and the only ascidian, Bostrichobranchus pilularis (Verrill), ranked sixteenth in order of numerical abundance but second in order of dry weight. This species accounted

THE BIOLOGY OF ASCIDIANS

35

for 0.26% of the fauna by number of individuals and 2349% of the total dry weight. One of the few estimates of the standing crop of ascidians on natural hard substrata was made by Gutikrrez and Lay (1965) who recorded Pyura chilensis at a density of 320 per m2with a mean individual weight of 350 g. Under favourable natural conditions Ciona intestinalis may attain population densities of 1 500-5 000 per m2 (Dybern, 1963), and Ascidiella scabra (Miiller) at Bohuslan, Sweden, 1 000 per m2 (Dybern, 1969b). C. Monniot (19654 records Microcosmus vulgaris at a density of several hundred per m2 on stones dredged from 120 m in the Gulf of Lions. It is evident that the group may form an important component in the fauna of some loose and solid substrates, and may sometimes play a significant or even dominant part in the economy of coastal waters.

B. Changes in populations Estimations of population density and biomass should take account of seasonal and year-to-year variations. Seasonal changes in the structure of the population depend on reproduction, growth and mortality, and have been referred to in sections 111 and IV, but little is known regarding the way in which ascidian populations vary over a period of years. Fouque and Franc (1953) noted that Ascidia mentula, Ascidiella aspersa and Ciona intestinalis decreased markedly on the shore near Dinard, France, within the space of one year, whereas Polysyncraton lacuzei Giard did not. In another part of the same region Molgula manhattensis declined from a very abundant species to a rare one. No explanation was found for these events but it is sornetimcs possible to relate faunistic changes with environmental changes, as for example when several species of ascidian penetrated to parts of the Rance estuary in France following dry summers (Fischer-Piette and Gaillard, 1950). And the appearance of Molgula manhattensis in the Caen canal was obviously made possible only by the increased salinity following the influx of sea water (Durchon, 1948). Some instances of this kind probably represent short-term fluctuations and species are generally in a state of dynamic equilibrium ;in other cases there may be a more lasting change. Carlisle (1954a)recorded a continued rise in the numbers of Trididemnum niveum (Giard) at Plymouth between 1951 and 1954 until in some places it had become the most abundant ascidian. He suggested that the species may have arrived from the French coast with the large brown alga Laminuria ochroleuca De La Pylaie and be increasing along with it. Certainly a few species, having found their way to new areas either by natural means or through human

36

R. H. MlLLAR

agency, rapidly become established. Styela clava Herdman was accidentally introduced to the south coast of England from far eastern waters, and multiplied until it became the dominant ascidian in some localities (Carlisle, 1954b ; Houghton and Millar, 1960 ; Stubbings and Houghton, 1964). Small numbers have been found recently on the French side of the English Channel and the species is expected to spread further along European coasts (C. Monniot, 1970). An instance ofemore local introduction is Botryllus schlosseri, first seen within the sluice-dock at Ostend, Belgium in 1960, having apparently been introduced on oysters imported from Holland; in the space of a few months it had reproduced and spread extensively (Polk, 1962). Even without human intervention the constitution of an ascidian population is not static and there is obviously e great need for longterm quantitative studies.

C . Factors affecting distribution and abundance The local distribution of species presents many ecological problems, and the striking differences in ascidian faunas of apparently similar habitats (Prenant, 1928) for the most part still await explanation. 1. Substratum The nature of the substratum is one of the factors determining the presence or absence of ascidian species, most of which either live attached to solid objects or are adapted to life on loose deposits. A few, however, have taken advantage of the fact that the test is a living and plastic tissue able to respond to differences in the substratum. Thus some specimens of Nicrocosmus sulcatus are attached by the base of the body to a solid object, but others develop rhizoids which form a network penetrating the soft deposit and securely anchoring the animal (Costa, 1960). An almost identical case was recorded by Savilov (1958) in the unrelated Chelyosoma mucleayanum Broderip and Sowerby. Responses to differences in the substratum and to other environmental factors may account for much of the variability so often noted in ascidians. For example P6rQs (1946) was able to relate the type of colony in Polyclinum aurantium to the sand-content of the water and to the space available. The remarkable plasticity of the body, and especially the test, enables the adult not only to modify its shape and mode of attachment but also confers a limited freedom of movement. Carlisle (1961) observed movement over the substratum in several species, in one case amounting to 8 cm in three months, and according to Lafargue (1968) Monniot found that colonies of Diplosoma would move away when

THE BIOLOQY OF ASCIDIANY

37

pricked by a needle. Behaviour of this kind may allow the animal to make adjustments of its position in response t o local changes such as the encroachment of other sessile organisms or displacement of the substratum. Most ascidians are fixed to a solid object, and although some seem to have little preference for organic or inorganic surfaces, others appear to be selective. Perhaps the success of Ciona intestinalis is partly due to a catholic taste in Substrata, for it lives on rock, shells and other inorganic things and also on Zostera and algae (Dybern, 1963). Several species of the family Pyuridae live on rocks and in addition on the hard cuticle-like surfaces of large brown algae, on dead calcareous algae, and on other ascidians with a hard superficial layer of test, but are not found on living calcareous algae or on soft brown algae (C. Monniot, 1965a). It is not clear whether this preference is determined solely by the hardness of the surface or by its chemical nature. In the Baltic Sea Styela eorincea uses the shells of living Astarte borealis in preference to stones (Dybern, 1969~). Many species of Ascidiidae, Botryllinae and Didemnidae frequently occur on living algae, and some like Aplidium pallidurn (Verrill) apparently prefer the surface of living plants. (One of the synonyms of that species-Aplidium zostericola Giard-refers to this fact). Of the species of the family Didemnidae occurring in a small area, Lafargue (1968) noted that two (Trididemnum delesseriae Lafargue and Diplosoma singulare Lafargue) required a flexible substratum, another (Diplosomalisterianum (Milne Edwards) ) occurred more frequently on flexible than on rigid supports, and the remaining eleven species lived on a rigid substratum or on both types. Amongst species attached to either algae or inorganic surfaces, there may be preferences for certain kinds of alga, and Dybern (1969b) found Ascidiella scubra (Miiller) t o be common on laminarians, fucaceans, Halydris siliquosa and Delesseria sanguinea, but not on polysiphonians and furcellarians. The abundance of some species is limited by local shortage of suitable hard substrata, as on parts of the Scottish coast where Ascidiella aspersa is moderately common but becomes very numerous when additional surfaces are placed in the water (Millar, 1961b). But even in the presence of suitable objects, it has been observed that the numbers of certain pyurids may be limited if the objects are far apart (C. Monniot, 1965a). Soft loose substrata present particular problems t o sessile animals, but numerous ascidians, of several families, have adopted this habitat, and three kinds of adaptation have evolved. The commonest is the production of test filaments, which penetrate the deposit and become coated with particles, thus effectively fixing the body in position

38

R. I€. Nm.T.AR

(Fig. lGa and b). Numerous examples are to be found amongst the Molgulidae, some in the Styelidae, and in the Pyuridae there are species in which this adaptation occurs only in individuals which happen to be on loose sediment (C. Monniot, 1965a). The second type of adaptation is the possession of a stalk with a a

C

mm

f Flo. 16. Adaptations to loose substrata. a, Bathyatyeloiclea enderbyanua ; b, Dicatpa pacibra; c , Polycatpa delta; d, Eugyra wrnbaeekae; e, Heteroatigma fagei; f, movemont of Heterostignra fagei amongst sand grains (c, redrawn from Monniot and Monniot, 1968; e, f, redrawn from Monniot and Monniot, 1981).

TEE BIOLOGY OF IWCIDIANS

39

tuft of basal filaments which anchor the animal (Fig. 16c and d). It may be more accurate to say that species with a stalk are able to take advantage of soft deposits, and that stalked rock-dwelling forms were pre-adapted for this habitat. Amongst the Pyuridae the short-stalked Pyura legumen Lesson living on hard inshore substrata may indicate the ancestral form from which P . bouvetemis (Michaelsen) evolved. In P . bouvetemis the development of filaments appears to be a response to the kind of substratum, for some specimens instead have a small basal plate (Millar, 1960), more suitable for attachment to solid objects. It haa been suggested that the stalk of P . bouvetemis may be too thin and flexible to support the body off the substratum (Millar, 1960),but Kott (1969) contests this view, and cites underwater photographs taken by the USNS " Eltanin " showing some specimens of the related P . georgianu (Michaelsen)with the body well above the sea-bed. Further striking examples of stalked species are the molgulid Eugyra aernbaeckae Millar, 1960, an Antarctic ascidian living in depths of 55-400 m, and the abyssal genus Culeolw. The third way in which ascidians have become adapted to life on soft bottoms is the more radical one of becoming interstitial animals. The discovery of interstitial ascidians was made by Weinstein (1961), who described Psammostyela delamurei, a small sand-dwelling styelid from shallow water in the Mediterranean. Since then a number of other species have been found in European waters (see F. Monniot, 1965,1966 for references) and one known species (Heterostigma separ drnbackChristie-Linde, 1924) has also been added to this ecological group (F. Monniot, 1966). Despite the systematic diversity-interstitial species are now known from the families Ascidiidae, Corellidae, Styelidae, Pyuridae and Molgulidae-certain features are held in common. F. Monniot (1966) has listed these as : small body size ; shape of body (flattened or, more usually, spindle-shaped), lack of pigmentation, mobility, incubation of embryos and a kind of neoteny. Mobility is perhaps the most noteworthy character. It results from a modification of the muscular activity which in attached ascidians merely achieves contraction of the body, but enables these specialized forms to creep amongst sand grains (Fig. 16e and f). Many species living on a loose substratum are neither interstitial nor stalked, but nevertheless are intimately affected by the nature of the sediment. Glkmarec and Monniot (1966) found a close relationship between the distribution of ascidian species and the granulometric composition of the soft sea-bed off Brittany, France, and concluded that ascidians are good ecological indicators of the nature of the sediment. The ascidian fauna of the Patagonian Shelf affords further evidence of

40

R. H. MlLLAR

the way in which the coarseness of the deposit affects the occurrence of species (Millar, 1960). Substrata which are classed as loose sediments may nonetheless have sufficient hard surfaces to support a population of species not adapted for living directly on sand or mud, as in the case of Ascidiella scubra (Muller) (Dybern, 1969b). Often such species make use of the shells of living molluscs, or the surface of benthic animals including other ascidians. In this way, for instance, Styela coriacea maintains a population in deep muddy areas of the Firth of Clyde, by growing on the upper valves of the mollusc Chlamys septemradiata (Miiller), 42% of which may carry the ascidian, to the number of 2-5 on each Chlamys (Allen, 1953). In the Baltic Sea the same species occurs on the shells of Astarte borealis, some 20% of which have at least one specimen (Dybern, 1969~). And Molgula manhattensis has been found attached to the siphons or shell of 23.5% of specimens of the bivalve Mya arenaria L. cast up on a beach in New Jersey, U.S.A. (Aldrich, 1955). The mesogastropod Trichotropis cancellata Hinds lives on unstable shelly substrata and its hairy surface provides attachment for at least three species of simple ascidian (Yonge, 1962). Appearances can sometimes be deceptive, when species normally confined to solid substrat.es are present on mud. Bouchet (1962) found Ciona and Ascidia mentula living on a soft muddy bottom and only on close examination realized that the animals were in fact attached to the roots of Zostera embedded in the bottom. Ascidians with a hard test themselves serve for the attachment of other ascidians, and 21 species have been found as epibionts on the test of Microcosmus sabatieri Roule on fishing grounds off Banyuls-sur-Mer, France (C. Monniot, 1965b). This large ascidian plays an important part in the ecology of the area, since together with its attached organisms numbering some 200 species it builds up large living complexes known as " blocs B Microcosmus ", which greatly influence the local productivity of the sea-bcd Thus

Fro. 17. Various methotls of attachment on looso substrata. a, Halocynthia papillosa; b, Polycarpa pornaria; c , d, MicrocoemuR ~ u l (redrawn ~ t ~from Costa, 1960).

THE BIOLOGY OF ASCIDIANS

41

Microcosmus effectively constitutes an extension of the rocky shore habitat on to the area of loose sediments and supports a rocky shore fauna. In contrast Halocynthiapapillosa L., another large free-standing ascidian, is devoid of epibiotic forms, possibly owing to its densely papillated test (Costa, 1960). Loose deposits may be sufficiently varied to provide a number of distinct micro-habitats within a single area and accommodate species of diverse requirements, as in the Bay of Marseilles, where the three large ascidians Halocynthia papillosa, Microc o s m ~sulcutus and Polycarpa pomaria (Savigny) have different relationships with the substratum, as indicated in Fig. 17 (Costa, 1960). In a detailed study of the fauna of coralline substrata off Banyuls Laubier (1966) listed the microhabitats of 21 species of ascidian. Only three were photophilic and ten preferred shade ; four lived as epibionts on other organisms-chiefly Bryozoa, hydroids and gorgonianswhereas eleven were attached directly to the hard substratum ; and a variety of preferences was shown for the upper, lateral or lower surfaces of objects. It is evident that, even with the small number of environmental factors considered, most species had a definable microhabitat.

FIQ.18. Distribution of Microcoanzw, aabatieri and M . v d g a r k near Banyuls. Vertical lines, 11.1. sabatieri very abundant ; light dots, M . eabatieri dominant ; horizontal lines, M . eabatieri and M . vulgarie; heavy dots, M . vulgarie abundant (redrawn from Monniot. 1965b).

42

R. € MILIAR I.

Local differences in the distribution of related species, but on a somewhat larger scale, were shown by a survey of the sea bed off Banyuls (C. Monniot, 1965b), where Microcosmus sabatieri and 111.vulgaris were dominant in adjacent areas defined more or less closely by contours of depth (Fig. 18). Numerous faunistic studies of sublittoral areas have given rise to the concept of biocoenoses, communities or associations, but whether or not such assemblages are held together by biological as well as physical factors (see Jones, 1950),it is generally agreed that they exist, and that they can usually be characterized by a set of species. P6rBs and Picard (1958) noted that certain kinds of sea-bed are rich in ascidians, and P&Bs (1967) included ascidian species amongst the animals characteristic of a number of biocoenoses in the Mediterranean. Of four biocoenoses recognized by Bellan et al. (1961) in an area off Corsica one was marked by the abundance of a species of Diazonu, and another was divisible into two facies typified respectively by Polyclinum aurantium Milne Edwards and by various compound ascidians together with Microcosmus sulcatw. Parenzan ( 1959) included eight ascidian species amongst the 47 animals characterizing one facies in the Gulf of Naples, and a Dendrodoa grossularia community has been recognized at Roscoff (Cabioch, 1961). 2. Salinity Ascidians in general are animals of rather high salinity water, although a number of species can withstand varying degrecs of dilution. Osmotic regulation takes place, but difficulties imposed by the large body surfaces, and by the absence of excretory tubules (Barrington, 1965)may restrict penetration into very diluted water. Ciona intestinalis is amongst the species with a wide salinity tolerance, and Dybern (1967) noted that it occurs in areas of the Black Sea having a salinity of under 20%, and also at Suez where the salinity reaches 40-41%,. The lower limit appears to be about 1I%,, both for the adult and the developmental stages, and Dybern's experimental results help to explain the distribution which he recorded around southern Scandinavia. In a similar way the local distribution of Ascidiella scabra (Muller) in the Skagerak and Kattegat is determined by a requirement for average salinities above 24%,, although the adult can withstand occasional reductions to 15%, (Dybern, 1969b). The prevailing salinity was also found to be the most important physical factor determining the presence or absence of a number of ascidian species in different parts of two marine ponds in Norway (Dybern, 1969a) (Table 111). Of these species Molgula munhttensis

43

THE BIOLOGY OF ASCIDIANS

certainly withstands salinities lower than the 23%, recorded since it has been taken from parts of the St. Lucie estuary, Florida, with values as low as lo%,,and even lower at certain tidal states (Gunter and Hall, 1963). Other species known to survive diluted sea water are Ecteinascidia turbinuta Herdman, found by Calder et al. (1966) at 22-47%, and Styeb coriacea which withstands 15%, (Diehl, 1957). S. coriacea and Dendroha grossularia live and breed in the Baltic Sea at a salinity of about 12%, (Dybern, 1969~). According to C. Monniot (1965s) pyurid species are excluded from areas with salinities below about TABLE111. LOWERLIMITSOF SALINITY TOLERANCE OF AVCIDIANS I N NORWEQIAN MARINEPOOLS ~~

Salinity

specie.¶ Clavelina lepadijormia Cwna inteatinalie Corella parallelogramma Ascidia callosa A . conchilega A . mentula A . virginea Ascidiella aapersa A . scubra * Dendrodoa grossularia *Styela ruatica Botrylloides leachi * Botryllua schlosseri * Boltenia echinata Molgula citrina M . manhatten& ~

~~

~~~

x0

14 12 18 30 30 20 20 18 18 20 20 16 23 26 17 23

~

Too few specimens to show clearly the salinity limits.

20%,. In certain places low salinity may preclude breeding owing to the sensitivity of the zygotes, embryos or larvae, while permitting the maintenance of the more tolerant adults. Such populations depend on recruitment by immigrant larvae during periods of higher salinity (Dybern, 1967, 196913). This may apply also to Ascidiella mpersa in the Norwegian ponds, for Knaben (1952) found that salinities below 28%, prevented the development of eggs. But even within a single species different populations show different ranges of tolerance, according to the prevailing salinity in which the adults have been living and this represents a phenotypic rather than a genotypic adaptation (Dybern, 1967, 1969b).

44

R. R. MILLAR

3. Temperature Water temperature is a major factor controlling the occurrence of ascidians but has been considered more often in relation to geographical than to ecological distribution ; in pwticular the ways in which it sets thc limits of distribution by influencing reproduction, have been examined (see Section 111, p. I)). Indeed, temperature is less likely to be a critical factor affecting local distribution than is either salinity or the nature of the substratum, but a few cases of local effects have been recorded. Low winter temperature killed Ciona intestinalis, Styela plicata and Molgula manhattensis but not Botryllus schlosseri in the lagoon of Venice, which has a great annual temperature range but is free from the complicating factor of fluctuating salinity (Sabbadin, 1958). In sheltered semi-enclosed areas and in docks, where great numbers of a few species may be present, it is often difficult to separate the effects of high temperature from those of other factors. But Naylor (1965s) observed marked changes in the numbers and the relative abundance of Ciona iatestinalis and AscidieEla aspersa in the docks at Swansea, Wales, following changes in the water temperature produced by the discharge of heated eMuent from a power station, over a period when other factors were comparatively steady. The response of the two species was complex and resulted in A. aspersa being dominant in winter and spring and Ciona intestinalis in summer and autumn. Effects of this kind depend less on lethal temperatures than on alterations in growth rates and the period and success of breeding (see Sections I11 and IV), although temperature limits for normal embryonic development (Runnstrom, 1929; Knaben, 1952) may determine whether a species succeeds locally. When temperature and salinity both vary, each may modify the effect of the other, but often the extremes do not coincide, and in that situation temperature may be less important than salinity (Dybern, 1969a). 4. Turbidity

Ascidians, being filter-feeding animals, are affected by the amount and nature of suspended matter in the surrounding water, but there are few observations to indicate the importance of this factor in nature. C. Monniot (1965a) discovered that at a depth of 90 m near Banyulssur-Mer a current of 0.5-1 knot raised clouds of sediment from the seabed on which pyurid ascidians were living. A moderate amount of suspended matter appeared to be beneficial, but too much led to clogging of the branchial feeding mechanism and subsequent death. In species bearing a rich epifauna, the death of attached organisms can damage the ascidians by encouraging pollution. Monniot also records

T H E BIOLOGY OF ASCIDIANS

45

the destruction of an abundant population of Ascidia sp. following disturbance of the sea-bed and increased turbidity. The importance of the silt-content is indicated by the presence of fewer ascidians in silty than clear water, on Scottish shores (Lewis and Powell, 1960). Moreover, the effect was more marked in the small compound forms, than in the large Ascidia mentula which withstood turbid conditions. Sediments rich in organic matter may favour certain species by ensuring adequate food in the overlying water, and the presence of Microcosmus sulcatus is said t o indicate such conditions (Carpine, 1964). 5. Light

The influence of light on ascidian larvae-r rather the spacial variation in light intensity-is well known (see Section III), and is one of the principal factors controlling micro-distribution. C. Monniot (1965a) reports that the distribution of Microcosmus sabatieri in the Gulf of Lions is strictly related t o the amount of illumination received, so that on the open sea-bed the upper limit is 15 m, on vertical surfaces facing south 7-8 m, and facing north 3-4 m, and on under surfaces 50cm. A survey of the Gullmar Fjord, Sweden, showed that C i o m intestimlis occurs sparingly on shallow horizontal surfaces, and about 75% of all specimens live on steeply sloping rock walls and overhanging ledges and in caves (Dybern, 1963). It is the larval choice of shaded places for settlement which determines this pattern of distribution, but although little is known of the effect of light on the adults, the development of strong pigmentation in individuals living in shallow unshaded areas (Dybern, 1963) suggests a need for protection from strong light. This is likely t o be more important in species with a thin transparent test than in those having a thick opaque test, and could have been one of the factors favouring the evolution of the ocellus and the associated shadow reflex of the larva which facilitates the choice of shaded areas. The direction of illumination may affect the orientation of the adult body. Ciona intestinalis has been observed t o grow in aquaria so that the long axis of the body and more especially the siphons, are aligned with the direction of the prevailing lighting (Millar, 1953a). I n nature the resulting posture will generally present the oral siphon to falling food particles and may also be useful in ensuring that the body grows up from the substratum. 6.

Biotic factors

The gregarious settlement of marine invertebrate larvae has recently received some attention (see Thorson, 1964 for references), and a few

46

R. H. B f I I L A B

ascidians have been cited as possible examples (Grave, 1935 ;Glaser and Anslow, 1949). Littoral species may be gregarious, but live in such a complex environment that it would be difficult for an observer to separate the results of gregarious behaviour from those of other phenomena. In the sublittoral region, however, a much simpler situation exists, and C. Monniot (19654 believes that the micro-distribution of a number of species points to gregarious settlement of their larvae. Thus Bolteniopsis prenenti Harant was found in isolated groups of 30-40 individuals. Microcosmus vulgaris Heller showed similar aggregations separated by apparently suitable areas which were unoccupied, and Molgula manhattensis, M . occulta Kupffer and Dendrodoa grossularia (Van Beneden) provided further examples. C. Monniot (1965b) further states that in the formation of the characteristic “ blocs Microcosmus” on the sea bed off Banyuls-sur-Mer, the first species to become attached attracts larvae of its own species and only later those of others. Lambert ( 1968) observed that larvae of Corella willmeriana Herdman tended to settle near adults, but the settlement of larvae close to adults is not in itself conclusive evidence of gregarious behaviour, because the adults may influence larval behaviour in the same way as inanimate objects projecting from the substratum, by altering the pattern of light and shade or the flow of water ;gregarious settlement concerns a response of the larvae to the presence of living adults of the same species. There is scope in this field for experiments, particularly as the larvae of some simple ascidims are readily obtained by artificial fertilization. Another biotic factor is suggested by an observation of Goodbody ( 196 1 b) that panels uscd in experiments on settlement failed to develop a normal community-of which ascidians formed a prominent partwhen placed close to mature sponge-anemone-ophiuran communities. Sponges were thought to be responsible, but the way in which they suppressed other communities is not known. We have seen that the nature of the sea-bed influences ascidians, but they themselves presumably have a significant effect on the surface which they populate if they are sufficiently numerous. Diehl (1957) noted the deposit of faeces on the surface of the sediment surrounding Styela coriacea ; and the clarification of turbid water by Ciona (Berner, 1944) involves the removal of suspended organic and inorganic particles from the water and their deposition on the bottom. A dense population of Ciona,such as that recorded by Elroi and Komarovsky (1961) may filter as much as 11 000 l/h over every m2 of substratum occupied, assuming the filtration rate determined in experiments by Goldberg et al. (1951). Even in the less dense populations more commonly occurring in this and other species, these animals must remove much

THE BIOLOGY OF ASUIDIANS

47

plankton from the sea and also contribute significant amounts of metabolites. A further influence which ascidians may have on their environment is in stabilizing a loose substratum, and many sand and mud-dwelling species have abundant test fibrils which bind particles of the surrounding deposit. The molgulid Bostrichobranchus pilularis is an example, in which the body is coated with mud. Moreover, specimens are loosely attached to one another (Van Name, 1945), and evidently constitute 8 living mat on the surface of the sea-bed. The abundance of this species in some areas (Abbott, 1951) suggests the important r d e which such ascidians may play in fixing soft deposits. It is more surprising to find ascidians playing a part in the formation of reefs, but Renouf (1937) has described how, together with sponges, they assist in cementing slabs and boulders on steep rocky banks of the shore. New techniques may assist advances in unexpected directions, and the increasing use of free diving methods has not only clarified the relationships of ascidians to their substratum but also helped in taxonomic studies. For example, Lafargue (1968) examined the didemnids of a limited area off the coast of Brittany, France, and her separation of a number of closely related species, using anatomical characters, is supported by differences of microhabitat in respect to depth, illumination, rigidity of the substratum, and proximity to sediment. Another aspect of local distribution which until recently has received little attention is the extent to which a single species may be divided into sub-populations. It is now known, however (Sabbadin and Graziani, 1967), that Botryllus schlosseri in the Lagoon of Venice has genetically controlled sub-populations existing under the same ecological conditions but a few miles apart. Similarly, sub-populations exist under different ecological conditions at the same location. It is possible that variations in the colonies of species of Didemnidae presbnt a parallel case, for the different forms tend to live in different microhabitats (Lafargue, 196 8). VI. PREDATORS, PARASITES,COMMENSALS AND SYMBIONTS c Organisms are associated in various ways, which have been discussed and defined by Cheng (1967). Predation, parasitism and commensalism are important aspects of ascidian biology and I have used these terms in accordance with Cheng’s definitions, but symbiosis, implying mutual metabolic benefit by associated organisms (which Cheng recognizes as mutualism) is apparently of little significance within the group.

48

R. H. MILLAR

A. Predators Predators are often recognized as such by the remains of their prey found during the examination of stomach contents. Only a few ascidians, however, have parts-the calcareous spicules and in some the test-which sufficiently withstand digestion to be identified. It is not surprising, then, that there are few records of ascidians forming part of the diet of commercial fish, and it may be largely for this reason that they are commonly regarded as distasteful. Thompson (1930, 1931) stated that ascidians are not of much general importance in the diet of fish, although Ascidiella scabra (Muller) sometimes is the chief item of food of the haddock in areas where both species are common. Rae (1956, 1967) also records the occasional presence of ascidians in the stomach of cod and lemon sole, the latter taking both solitary and colonial forms. Some West Indian fish frequenting coral reefs eat " tunicates '' (presumably ascidinns), which constitute 10-28% of the stomach contents according to the species of fish (Randall and Hartman, 1968).

Amongst animals with a very varied diet, crabs are known to take ascidians. Bancroft (1903) found that colonies of Botryllus schlosseri in aquarium tanks at Naples were eagerly attacked by crabs, but Botrylloides leachi was soon rejected and the crabs quickly recognized it as distasteful. The relatively constant appearance of Botrylloides leachi may help would-be predators in learning t o avoid the species ;the colour pattern of Botryllus schlosseri by comparison is very variable. Beaven (1956) described how a single Blue Crab (Callinectessapidus) accidentally confined in a cage along with young oysters and Molgula mnhattensis apparently ate all the ascidians in preference to the oysters. The conditions were, admittedly, unnatural as they are in most feeding experiments, but the observation at least indicates that ascidians may be taken in nature on quite a large scale. According to Goodbody (1963a), polychaetes probably fed on young specimens of Ascidia nigra which he had under observation. Starfish have rarely been recorded as predators of ascidians, but are known to be the chief enemies of Pyura chilensis Molina (Gutihez and Lay, 1965). It is amongst the molluscs that some of the main enemies are to be found, or at least they are more frequently recorded, but in part this results from their being less active, spending more time in attacking their prey, and being therefore more readily observed. Of the prosobranch gastropods Erato voluta (Montagu) feeds on Botryllus schlosseri and Botrylloides leachi, inserting its proboscis through the oral siphon of the zooid (Fig. 19) (Fretter, 1951), and several other species of the

THE BIOLOGY OF ASCIDIANS

49

molluscan super families Lamellariacea and Cypraeacea appear t o prefer ascidians to other prey (Fretter and Graham, 1962). Lamellaria perspicua (L.) possibly lives entirely on colonial ascidians. Velutina velutina (Miiller) attacks Ascidia a n d a pyurid species (Ankel, 1936) and Diehl (1956) has described how it bores through the test of Styela wriacea remaining with its prey for about 2 days until nothing remains but an empty test. This gastropod also lays its eggs on the ascidian and appcers to spend much of its time in association with it. Fusilriton oregonensis feeds on Halocynthia aurantium (Pallas), both in the field and laboratory (Smith, 1070), although this ascidian is believed t o be relatively free of prcdators. Milkman (1967) found that the snail Mitrella lunata attacked Botryllus schlosseri grown in laboratory

FIG.19. Ercrto volutu feeding on BotryZlua schloeaeri (redrawn from Frettor, 1951).

culture vessels, and it probably also does so in nature. The opisthobranch gastropod Pleurobranchus membranaceus (Montagu) preys on both compound and solitary ascidians. Yonge (1949) has described how it waits until the ascidian opens its siphons, then quickly thrusts the proboscis in and feeds on the soft tissues, but it also has other methods of attack and may bore through any part, of the test of large ascidians (Thompson and Slinn, 1959). A number of nudibranch molluscs (Goniodoris nodosus (Montagu), G. castanea Alder and Hancock and Ancula cristata (Alder))feed on the colonial Diplosomu listerianum, Botryllus schlosseri and Botrylloides leachi, and on the solitary Dendrodoa grossularia. Idulia elegans also attacks the solitary Polymrpa pomuria (Savigny) (Hoffmann, 1926). An interesting parallel t o the feeding habits of these gastropods is to be found amongst the turbellarian flatworms, some of which habitually feed on ascidians. Cycloporus papillosus Lang attaches itself t o colonies of Botryllus and Botrylloides, by its ventral sucker, and, in-

60

R. € MrLLAR I.

serting its pharynx within the colony, extracts whole zooids which pass intact into the gut (Jennings, 1957). Where the prey is larger, as in the solitary species Corella willmeriana Herdman, the flatworm Eurylepta leoparda Frceman enters the branchial sac before attacking the tissues, rolling itself into a tubular shape to pass through the oral siphon (Lanibert, 1968) ; after 3-7 days only the test remains. Experiments made by Lambert suggest that this flatworm feeds only on Corellu willmeriana and refuses other solitary and colonial species. This recalls earlier work by Crozier ( 19 17), who found that specimens of Pseudoceros crozieri would feed only on the species of ascidian with which they had previously been associated. Finally, amongst the mammals, the Grey Seal has been noted t o take ascidians (Rae, 1968), although these probably form a very small part of a varied diet. Man can also be included amongst the predators since some of the larger ascidians are collected for food in the Mediterranean and Chile (Harant, 1951) and in Japan (Tokioka, 1953). If an ascidian is common and large it is sometimes used for bait, as in the case of Pyura praeputialis (Heller) in Australia (Hedley, 1915)) where local populations may be depleted by fishermen (Pope and McDonald, 1968). In South Africa a few species also serve as bait (Harant, 1951). Apart from such deliberate gathering, large quantities of ascidians must be destroyed accidentally in the course of commercial fishing, and where they are regarded as pests, as on oyster beds, they may be systematically dredged and destroyed (Cole, 1956).

3. Commensals, parasites and symbionts It is generally a fairly simple matter to decide if one animal preys upon another, but other kinds of association between species-phoresis, commensalism, mutualism and parasitism-are often difficult to distinguish in practice. No doubt most cases of such association could be classified if the physiology of the partners had been studied, but such studies involving ascidians are rare. Many instances of commensalism are known in which ascidians act as the hosts, and their suitability is doubtless due to the large branchial and atrial cavities, the filter-feeding habit which brings continuous supplies of food and water, the relative ease of entry to the cavities, and the absence of effective defensive mechanisms. The Crustacea contain some of the best known commensals, of which the notodelphyid copepods are particularly widespread. Species of this family are almost exclusively associated with ascidians. Schellenberg (1922) listed 89 species, and others have since been added (Illg, 1958 ;Illg and Dudley, 1961, 1965). Little is known of the effect of these

51

THE BIOLOOY OF ASCIDLANS

copepods on their host, but the presence of large numbers can scarcely be without some effect ; Illg (1958) took about 300 specimens of a species of Doropygus from the branchial sacs of 20 specimens of an ascidian in addition to 28 amphipods, five polychaetes and two pinnothcrid crabs from the branchial or atrial cavities. And, according to Gotto (1067), several individuals of Notodelphys allmuni often inhabit even small specimens of Ascidiella aspersa. Moreover some of the copepods are quite large in relation to the cavity they inhabit, and a single specimen may occupy fully half of the branchial sac (Gotto, 1961). Nevertheless, the host generally shows no sign of ill effects, and Corella parallelogramma infected with Ascidicola rosea Thorell appeared to survive, feed and spawn as well aa uninfected specimens (Gotto, 1957). This suggests B long-established evolution of the commensal species in association with the host species. Adaptation is evident in the life cycle of this copepod, for the female bearing fertilized eggs movcs from the ascidian’s oesophagus to the stomach, where the eggs are deposited and hatch, but the nauplii retain the inner egg membranes while passing through the ascidian’s intestine and rectum, being freed from the membranes only after leaving the anus (Gotto, 1957). An opposite migration by the ripe females, from the stomach to the branchial sac, occurs in another ascidicolous copepod, Enteropsis sphinx (Aurivillius), whose nauplii are presumably released through the oral siphon (Gotto, 1961). Another adaptation by a commensal is the timing of breeding in Ascidicola rosea Thorell, which produces its larvae when a newly settled generation of the host Ascidiella aspersa is established and can be infected at an early stage (Gage, 1966). Although many copepods live as commensals in ascidians, others have adopted a more or less parasitic existence, some in cysts within the tissues or blood vessels, but the life histories are almost entirely unknown (Illg, 1958). One of the most remarkable is Gonophysema gullmarensis Bresciani and Lutzen (Fig. 20), a species living in the body wall of Ascidiella aspersa, surrounded by a blood space from which the parasite, lacking both mouth and gut, presumably obtains its nourishment (Bresciani and Lutzen, 1960). Since the average number of parasites in a host appears to be about three, however, and the size only from 1-8 mm, little damage may result. The parasite is surrounded by a thin membrane of host tissue, indicating some reaction on the part of the ascidian. But the colonial Distaplia unigerrnis Ivanova-Kazas has no detectable reaction to the presence of parasitic copepods (Ivanova-Kazas, 1966). In addition to the Notodelphyidae, the copepod families specially associated with ascidians either as commensals or parasites are the A.M.B.--B

3

52

R. H. MILLAR

Lichomolgidae, Archinotodelphyidae, Ascidicolidae and Enterocolidae. In these, certain specics occur in several ascidians, but others appear to be much more host-specific (C. Monniot, 1961, 19658). C. Monniot (1961) has also found that some of the copepod species characteristically occupy particular parts of the branchid sac and that there appears to be no antagonism between species occupying the same host. What factors determine the incidence of commensalism or parasitism, and whether there is any chemical attraction leading to infection are unanswered questions. At.

‘Pb .

.

FIQ.20. Gonophyaema gullmarensia in the body wall of Aacidielln nsperaa. 8. with egg sacs protruding int.o tho atrial cavity ; b, soen in a transverse section of the branchid region of tho ascitlian (redrawn from Bresciani and Liitzen, 1960). At., atrium; G., gonad of parsuite; Ph., pharynx.

A few amphipods are commensal in solitary or colonial ascidians (Harant, 1931) and infection may amount to almost 100% of the host species (C. Monniot, 1965a). Amongst the decapods also there are instances of commensalism. Several species of Pontonia are reported from solitary ascidians (Oka, 1915; Kemp, 1922; Sluiter, 1927). In view of the large size of the crustaceans these authors considered that the host was entered only by the larval Pontonia, but Harant (1931) found that adult P . $avomaculata Heller taken experimentally from Ascidia mentula and Phallusia mammillata repeatedly made their way back into the branchial sac. This ability, together with the apparently unsuitable food which the crustacean would find in the branchid sac (Sluiter, 1927) suggests that Pontonia may shelter within the ascidian and leave it at intervals to make feeding excursions. It would be interesting to investigate how

THE BIOLOGY OF ASCIDIANS

53

the ascidian reacts when the Pontonia enters its siphon, which would normally close on being stimulated. But if the ascidian accepts its guest, what is the advantage to the host? It is striking to see, as I have, specimens resembling a Pontonia, of length 2-7 cm, in the branchial sac of Ascidia interrupta itself only 7.3 cm long (Fig. 21). Also amongst the decapod Crustacea a few species of the pea-crabs Pinnotheres have adopted the branchial sac of simple ascidians as their residence (Harant, 1931 ; Salfi, 1939 ; MacGinitie and MacGinitie, 1949).

Fia. 21. Aaridin interrupfrc with a large commonsel. possibly a species of Z'onfonin, in tho branchial sac.

Although nothing is known of the host's reaction, there is some evidence that the pea-crabs and the amphipod Leucothoe spinicarpa will tolerate each other, but will not accept the alpheid Pontonia flavomaculata (Harant, 1931), and i t would be surprising if some sort of exclusion did not take place in the restricted micro-habitat offered by an ascidian branchial sac. Few molluscs live as commensals with ascidians, the best known being the bivalve Musculus marmoratus (Forbes) found in the test of Ascidia mentula and less commonly Ascidiella aspersa and other European species. Brewin (1946, 1948) records the presence of mussels from several species of ascidians in New Zealand. Another was found in the test of Herdmania momus (Savigny) (Das, 1938), over 40 individuals sometimes inhabiting a single specimen.

54

R. H.MILLAR

Bourdillon (1950) found that the mussel does not penetrate the test of its host, but merely makes a depression by pulling the shells down after attaching byssus threads. The mussel is apparently not attracted by the ascidian, but preferentially settles down on the test following an accidental encounter. The bedding reaction, however, is probably a response to a chemical factor of the test, since it occurs even when an eviscerated test is offered. There can be little question of mutual benefit from the association, and the ascidian tolerates the mussel without suffering by its presence. A few gastropod molluscs have adopted a similar home in the ascidian test (Harant, 1931). C. Monniot (1965a) found polychaetes in the cloacal cavity of Microcosmus multitentaculatus Tokioka and the nemertine Tetrastemma vittatrtm in 90% of Microcosmus sabatieri Roule collected at Banyulssur-Mer. As already mentioned in relation to copepods, the distinction between commensalism and parasitism is difficult to establish, but undoubted parasites of ascidians are numerous amongst other systematic groups (Harant, 1931 ; F. Monniot, 1965) although we still know little of the effect on the host or of its response. One hydroid species, Endocrypta huntsmani (Fraser) has been reported from the branchial wall of ascidians (Fraser, 1937). What is often termed symbiosis, and more strictly mutualism, implies some degree of metabolic dependence between the partners. Droop (1963) has reviewed the significance of relationships between certain animals and symbiotic algae, and both he and Yonge (1937) pointed out that these animals usually have intracellular digestion. The fact that in ascidians digestion is extracellular may explain why they so seldom have symbiotic algae. Smith (1935) found that a number of tropical species of Didemnidae have algae in the cloacal cavities or the test, but doubted whether the ascidians could benefit from the association. PBrits (1960) also described algal cells in a species of Trididemnum from the Red Sea and Tokioka (1967) found zoochlorellae in lacunae of the common test of Trididemnum cyclops Michaelsen from the Gilbert Islands, and embedded in the test substance of T . v i d e (Herdman) from the Philippine Islands. In the last named species the zoochlorellae are apparently surrounded by the densely packed calcareous spicules of the test and it is uncertain if efficient photosynthesis would take place in such a situation. The following Indonesian didemnid species are also reported to have zoochlorellae in spaces of the test (Tokioka, 1967): Lissoclinum patella (Gottschaldt), Lissoclinum pulvinum (Tokioka), Diplosoma virens (Hartmeyer). A remarkable case was found by

THE BIOLOQY OF ASCIDIANS

55

Eldredge (1967), in which the larva of Diplosoma virens (Hartmeyer) was seen to have special pouches filled with conspicuous green algae ; the anatomical modification of the larva suggests that the relationship here is regular and possibly of mutual benefit.

VII. GEOGRAPHICAL DISTRIBUTION Many factors must have played a part in determining the present pattern of geographical distribution of species. Changes in the positions of land and sea masses during geological times were undoubtedly important, and have been used for instance to explain the widespread occurrence of certain species in the West Indies, Mediterranean and Indo-Pacific (Huus, 1927). Hydrographic conditions, too, have varied and may have influenced speciation and the isolation of species (Knox, 1963). The biological characteristics of the group have also to be taken into account. Amongst these is the short pelagic life of the larva which restricts dispersal, and Huus (1927) has shown that few ascidian larvae could be expected to survive oceanic transport over distances greater than 500 km. Transport on driftwood and algae, and in recent times on ships, is a more likely means of dispersal across wide and deep seas. The spread of species along coastlines, however, is less subject to restrictions imposed by larval biology and will be limited chiefly by the occurrence of unfavourable features in the environment, such as unsuitable substrata, temperatures which do not permit breeding, and other factors discussed elsewhere in this review. Studies of the zoogeography of ascidians are rather few. One of the most detailed was made by Hartmeyer (1923, 1924) who analysed the ascidian faunas of the Arctic and Boreal and interpreted them in relation to hydrographic conditions. The papers by Thompson (1930,1931,1933, 1934) were in part a translation of Hartmeyer’s work to which were added records from Scottish and adjacent waters. Huus (1937) included a review of world distribution in his major work on ascidians, PQrks (1958) has dealt with Mediterranean species, Oka (1935) and Tokioka (1963) with those of the Japanese seas and Kott (1969) with the Antarctic species. I n addition, many taxonomic papers describing collections from diverse areas give some consideration to questions of distribution and faunistic affinities. One of the principal obstacles to resolving questions of geographical distribution, faunistic relationship, and the origin of faunas is the unequal effort which has been made in different regions. The ascidians of several areas are now quite well known, but for certain large and important regions information is scanty. This is particularly SO in the waters of the Indian peninsula, and much of the Pacific and Atlantic

56

R. 11. MILLAR

coasts of South America. Moreover, the accounts of these faunas which have been extensively studied reflect the varying viewpoints of different systematists, some of whom have been more ready than others to create new species. A. Shallow-water ascidians Assuming that most of the species are now known in the areas which have been reasonably well studied, it is of interest to look at the relative richness of the faunas. In doing so it is necessary to compare like with like, by taking areas defined by the homogeneity of their faunas and having regard to the hydrographic conditions, sudden changes in which, over a short distance, often determine faunistic boundaries. Figure 22 shows the approximate number of ascidian species believed to occur in the main shallow-water zoogeographical regions. The regions are broadly those defined by Ekman (1953), but with some local modifications adopted by students of particular areas. It is evident that certain faunas are much more diverse than others, the Mediterranean, Indo-Malayan, southern Japanese and northwestern Pacific faunas being notably rich in species, the polar seas, subantarctic and temperate North American Atlantic less so, and in general the warm-water faunas have most species, although not necessarily most individuals. It should be noted, incidentally, that the total number of species throughout the world is not the sum of the numbers of all the regions, because by no means all species are confined to one faunistic area, many being shared by adjacent or even by several more distant areas. The warm-water regions, which will be considered first, are remarkable both for their richness and for the number of species of wide distribution. And some genera, such as Eudistomu, although not confined to warm regions, find by far their greatest development there.

Indo- West-Pacijc This is a very large region comprising the coasts of the Indian Ocean, the Indonesian archipelago, the western Pacific north to about Tokyo, and the northern, as well as much of the western and eastern coasts of Australia. Although relatively homogeneous, the region can be divided into a number of faunistic areas. Southern Japan The ascidian fauna of Japanese and immediately adjacent waters is very diverse, Tokioka (1963) having listed 277 species. These are divisible into four faunistic groups :

I

Scale: no. of species

I50 I

Fro. 22 Estimated number of species of ascidians in the main zoogeographical areas, but escluding abyssal species. A, Southern Japan; B, Indo-Malaya ; C, Western Indian Ocean ; D, Red Sea ; E, Northern Australia (Damperian); F, Northern .Australia (Solanderian) ; G, Eastern Australia ; H, South-eastern Australia (Maugean); I, Southern Australia (Flindersian) ; J, Southwestern Australia (Baudinian); K,tropical West Africa ; L, tropical and subtropical American Atlantic ; 31, Mediterranean ; N, tropical and subtropical American Pacific ; 0, boreal European Atlantic ; P. boreal American Atlantic ; Q, temperate north-eastern Pacific ; R, tempcrate north-western Pacific ; S, Arctic ; T,Antarctic ; U, Antiboreal South American ; V, Kew Zealand (Aupourian) ; W,New Zealand (Cookian) ; X,New Zeeland (Forsterian); Y, South Africa (south coast); Z, South Africa (Namaqua).

cn

4

68

R. H. 1. 2. 3. 4.

MILLAR

northern cold water species (north of Hokkaido and Korea); cosmopolitan species ; north-temperate species (all four main islands) ; warm-water species (southern part of Honsyu Island).

Some 74% of the total occur in southern Japanese waters, although only about 18% are strictly warm-water species belonging to the warm Indo-West-Pacific faunistic region and not extending north of the middle of Honsyu Island. These results confirm and amplify the earlier work of Oka (1935), who distinguished between the northern and southern elements in the endemic ascidians of Japan. The faunistic boundary passing through Honsyu Island corresponds closely to an abrupt change in the temperature regime brought about by the opposition of cold south-flowing and warm north-flowing currents, and emphasises the importance of temperature in determining distribution. The occurrence of 16 species in both southern Japanese and West Indian waters (Tokioka, 1963) is a remarkable example of the wide distribution of tropical ascidians.

Indo-Malaya The sub-region extending from the Indian sub-continent to the southern coasts of China, and including the Malay archipelago, is known to be one of the richest in species of any part of the seas. Unfortunately the collecting effort has been very uneven, relatively little being known of the ascidians of Indian waters, whereas those of the Malay archipelago and neighbouring waters have been well studied, principally by Herdman (1881, 1882, 1886), Sluiter (1885, 1904, 1905, 1909), Van Name (1918) and Tokioka (1950, 1955, 1967). As always, it is difficult to arrive at the total of good species in the area, but I estimate that there are about 178 already described. Allowing that less intensive collecting has been done there than in southern Japanese waters, the islands of Indonesia must be regarded as comparable in richness. Nevertheless there may be marked local differences in numbers of species and individuals as Van Name (1918) found in the Philippine Islands. Only statistical analysis of the results of planned collecting would show whether such differences result from inadequate sampling or are real and relate to local variations in habitat. Western Indian Ocean Many fewer species are recorded for the western part of the IndoWest-Pacific, which includes the eastern African coast and the islands of the western Indian Ocean. The area has been but poorly investigated,

THE BIOLOQY OF ASCIDIANS

59

and the papers by Michaelsen (1918, 1919a, 1920a) remain the chief source of information, but it may well be true of ascidians, as of other groups, that the western part of the Indo-West-Pacific region is significantly poorer in species than Indo-Malaya.

Red Sea About 53 species of ascidian are known from the Red Sea and the results of Michaelsen (1919b, 1920b) and Kott (1957b) demonstrate only a small endemic element. The occurrence of the majority of species also in other parts of the Indo-West-Pacific, as far eastwards as Indonesia and northern Australia, emphasizes the essential unity of the ascidian fauna of this large region. The modest number of species in the Red Sea may be partly a result of rather uniform and extreme environmental conditions. North-west, north and north-east Australia The northern coastal waters of Australia, from about 29'5 in the west to about 33"s in the east, support a warm-water and tropical fauna. The Torres Strait divides this coast into an eastern (Solanderian) and a western (Dampierian) province, each with perhaps about 50 species. Despite the evidence from echinoderms that these provinces have distinct faun= (Clark, 1946), there is some doubt whether ascidian distribution supports the clear separation. Analysis of Kott's (1957a, 1962, 1963) results shows that 20% of the species examined occur in both provinces, but this low figure may be due to the scarcity of records, since more complete collections from the northern coast (Kott, 1966) indicate that 76% of the species occur in both provinces. Kott (1966) found a strong relationship between the ascidian faunas of northern Australia and those of Indonesia, the Philippines and Japan. Only the Didemnidae provided species with a range extending across the Indian Ocean to the east African coast ; it may be significant that this is, systematically, the most difficult of all ascidian families and therefore the one in which there may be the greatest temptation to place specimens in species known to occur in other parts of the region. The fauna of the southern coasts from about Perth to Sydney is distinct and shows some a0inity with that of New Zealand and even with cooler more southerly areas according to Kott (1963), who also found evidence of subdivision of the south coast ascidian fauna. Tropical and subtropical West Africa The strictly tropical fauna of West Africa appears to extend from about 15"N to 15'5, and a related subtropical Mauretanean fauna from

60

R. H. MILLAR

15”N to the Straits of Gibraltar (Ekman, 1953). Over 70 species are known from the tropical part (Michaelsen, 1915; Millar, 19538, 1965), and although this relatively small number may be to some extent the result of incomplete knowledge it nevertheless indicates less favourable conditions than those of tropical areas of the Indo-West-Pacific region. Michaelsen (1915) did not stress a faunistic connection between the Guinea fauna and that of the West Indies, but Millar (1953b) found a collection of ascidians from Ghana to consist of a large endemic element, a small pan-tropical element and a small but interesting element comprising species also recorded from the West Indies. A similar result was shown by material from the “Atlantide ” Expedition (Millar, 1965),and PQrAs(1949) noted that 25% of the ascidians which he examined from Senegal were also known from the West Indian area.

Tropical and subtropical American Atlantic Hydrographic conditions indicate Cape Hatteras (35ON) as the northern limit of the eastern American warm-water region and a point south of Rio de Janeiro as the southern limit. Over much of the southern part of this area, however, the fauna is poorly known and it is difficult to determine how closely the faunistic boundaries correspond to the hydrographic ones. My estimate of about 83 species is based on the accounts of Van Name (1945), Rodrigues (1962, 1966) and Millar (1958b, 1961a, 1962~). This is only a modest fauna for a warm-water region, being scarcely greater than the relatively poor ascidian fauna of West Africa, and contrasts with the richness of other systematic groups. It has already been noted above that several species are common to the warm-water faunas of the western and eastern Atlantic. The Mediterranean Although geographically the Mediterranean looks like an entity, hydrographically and faunistically it is not sharply separated from the eastern Atlantic. This has long been recognized in other animal groups, and was confirmed by PQrAs(1958,1967)for the ascidians. He listed 130 Mediterranean species, of which 32% occur also in the temperate part of the Atlantic. More than half of these Atlanto-Mediterranean species do not extend into the eastern basin of the Mediterranean and are presumably Atlantic in origin. Within the Mediterranean there is a marked faunal division between the western and eastern basins, confirmed by the low percentage of ascidian species known from both basins. But half of all the species are endemic, and the fact that this proportion is much higher than amongst hydroids is explained by P&As

THE BIOLOGY OF ASCIDIAXS

61

as a result of the shorter pelagic life of ascidians. The remainder comprises mainly small numbers of widespread species, and species occurring throughout warm waters. Only one species is common to thc Mediterranean and thc Rcd Sea.

Tropical and subtropical American Pacijic From the Gulf of California in the north to about 4"S,on the coast of Peru, a warm-water fauna exists, part of which is tropical. The difficulty of fixing the northern limit of the region, for ascidians as for other groups, has been noted by Van Name (1945),and is due to the presence of cool water quite close to the coast far south on the Pacific side of the United States. However, it is established that the Gulf of California has a tropical ascidian fauna (Ricketts and Calvin, 1939). The southern limit of the region is not precisely known because the fauna is insufficiently described. The total of about 45 species indicates a poor fauna. Few of them other than circumtropical species occur also in the Atlantic American area. In other animal groups, including crabs and echinoderms, although the percentage of species common to the Atlantic and Pacific sides of Central America is also small, there is a substantial number of shared genera. Such comparisons of genera have little significance in ascidians, since most genera are of very wide occurrence. Boreal European Atlantic The whole temperate North Atlantic could be taken as a faunistic unit, but the eastern and western sides are sufficiently distinct to be considered separately. On the European coast the northern and southern limits are approximately the North Cape in Norway and the western end of the English Channel. The papers of Hartmeyer (1923,1924) and hback-Christie-Linde (1922,1923, 1928, 1934)remain the major zoogeographical accounts of the European boreal ascidians, and subsequent work (Thompson, 1930, 1931, 1932, 1934;Millar, 1966c) has done little more than fill in certain details. The total now stands at about 74 species, and although new species will doubtless be found, particularly from specialized habitats not hitherto examined in detail, it is not to be expected that the list will be greatly lengthened. The ascidian fauna is considerably poorer than that of the Mediterranean with its 130 species, although as we have seen the Mediterranean is not faunistically sharply cut off from the Atlantic. Few ascidians are strictly endemic to the European boreal region, and most of those which are centred there extend either northwards some way into the Arctic or southwards as far as the western basin of

62

R. H. MILLAR

the Mediterranean. Polyclinum aurantium, Aplidium nordmanni, Corella parallelogramma, Pyura tesselata and Microcosmus claudicuns are perhaps the species most nearly endemic, since none extends into the Arctic and, although all occur in the Mediterranean, P6rBs (1958) notes them as rare. Boreal species living on the continental slope may penetrate southwards beyond the latitudinal limit applying in littoral and inshore areas. Thus at depths of a few hundred metres in the Bay of Biscay an ascidian fauna exists which has more affinity with that of Scandinavia than with the fauna of the adjacent French coast (C. Monniot, 1969). Amongst the large Boreal-Mediterranean and Arctic-Boreal elements the limits for individual species in some cases at least appear to depend on temperatures which limit breeding (Millar, 1954a, 195413). A number of European ascidians are known also from the western Atlantic. Many of these are northern species with a more or less continuous distribution including Iceland and southern Greenland. The bridge formed by these islands together with the Wyville-Thompson Ridge accounts for the presence of species on each side of the otherwise impassable barrier of the deep Atlantic Ocean (Huus, 1927, 1936). Huus and Knudsen (1950) remarked that all of the 33 species known from Iceland, with a single exception, occur also on both the western and eastern sides of the Atlantic. Similarly, Lutzen (1959) showed that a high proportion of ascidians from Greenland are also known from both European and American coasts, although only some penetrate southwards into European boreal waters. Within the region the Baltic Sea constitutes an area of highly specialized conditions, characterized by the low and variable salinity. As noted elsewhere (p. 42) few ascidians can withstand very reduced salinities, and their limited powers of osmotic and ionic regulation (Barrington, 1965) account for a failure of the group as a whole to penetrate much beyond the transitional zone of the Belt-sea. Thus only three out of ten species collected from the Oresund and Kattegatt extended to areas of markedly reduced salinity (Millar, 1959b), and Dybern (1967)states that of about 30 species in the more saline approaches to the Baltic only three can be found in the southern Baltic proper. The distributional maps of Hartmeyer (1923, 1924) confirm the poverty of the Baltic ascidian fauna.

Boreal American Atlantic Ekman (1953) accepts Cape Hatteras as approximately the southern limit of the temperate fauna of the Atlantic coast of North America. The northern limit, although more difficult to establish, is taken to be

THE BIOLOGY OF ASCIDIANS

63

somewhere near Cape Cod. The ascidian fauna of the region is an impoverished one and includes only about 46 species. A number of these are common to both sides of the Atlantic, and Huus (1927) noted that 24 of the 28 European boreo-arctic species but only 4 out of 46 European boreal and south boreal species occur also on the American coast.

Temperate north-euatern Pacijic The Pacific coast of North America, from lower California to the Alaskan peninsula, forms one faunistic unit, with more or less distinct subdivisions, and Van Name (1945) distinguishes an element centred on the coast of northern California and another on the coast of British Columbia. Water along most of the coast is rather uniform in temperature. The ascidian fauna is not rich, with only about 43 species (Tokioka, 1963), several of which occur over a large north-to-south range. Tokioka contrasts this with the richer fauna of the north temperate waters of the western Pacific, and notes in particular the scarcity of species of Pyura and the absence of Polymrpa, Microcosmus and the subfamily Diazoninae on the American side. Temperate north-western Pacijic The coastal area from about the middle of Honsyu Island, Japan northwards to the eastern coast of the Kamchatka Peninsula constitutes one faunistic region, occupied by temperate and cool-water species. Within this area some 73 cool-water species, and 152 north temperate-water species of ascidian are recorded (Tokioka, 1963), representing a very rich fauna. A number of these occur also on the Pacific coast of North America. Arctic The whole of the Arctic is a fairly homogeneous zoogeographical unit, with only partial longitudinal division into areas having distinct faunas. Hartmeyer (1904) noted this with regard to ascidians, and confirmation is found in subsequent work by Hartmeyer (1923, 1924), h b a c k (1922, 1923, 1928, 1934) and Van Name (1945). The distributional maps in Hartmeyer’s account of the Ingolf Expedition show how commonly Arctic species, especially those of the high Arctic, have a circumpolar distribution. There appear to be about 80 species of Arctic ascidians, and the fauna is not only quite rich in species but locally very rich in individuals. MacGinitie (1955) and Abbott (1966) found them to be one of the dominant groups of marine invertebrates at Cape Thompson, Alaska. In any given area the ascidian fauna itself

64

R. 11. MILLAR

is oftcii dominated by a few species, as in the Canadian Arctic, whcrc of 27 ascidian species identified, thrcc (Boltenia ovifera, Boltenia echinnla and Ascidia callosa) accounted for about half of all specimcns collccted (Trason, 1964). The Arctic ascidian fauna is, naturally enough, most closely allied to that of the colder parts of the boreal regions of the Atlantic and Pacific Oceans; and the eastern Pacific shows more afinity to the Arctic than does the western Pacific (Tokioka, 1963). The land mass encircling much of the Arctic Ocean can account for the relatively uniform nature of the fauna, but for the gap made by the North Atlantic and the Greenland Sea. The submarine ridges linking northern Europe, the Faeroes, Iceland and Greenland may have formed a bridge across which species could pass (Huus, 1927, 1936), but Liitzen (1959) suggests an alternative or additional route of ascidian migration, by way of the unbroken shelf bordering the north polar sea, possibly during periods when the Arctic was less cold than now.

Antarctic The Antarctic region is one of the most clearly defined of the worlds zoogeographic divisions, and its northern limit coincides rather closely with the abrupt change in water temperature indicated by the Antarctic Convergence. It is distinguished, too, by the sudden increase in depth at the edge of the shelf, and the Antarctic shelf fauna is in consequence somewhat isolated from neighbouring shelf faunas. Two divisions have been recognized : the high-Antarctic sub-region consisting of the continental coastal area and the low Antarctic sub-region including South Georgia and Shag Rock Bank (Ekman, 1953). Knox (1960) accepts these provinces, but Kott (1969) in dealing with Antarctic ascidians takes the South Georgian province to include the Bellingshausen Sea, the Antarctic Peninsula, and the South Shetland, South Orkney and South Sandwich Islands. The shelf fauna of the region contains about 73 ascidian species, this total being based on the most recent accounts by Vinogradova (1962a) and Kott (1969), but excluding some doubtful species. In other invertebrate groups most species seem to occur fairly generally in suitable habitats around the continent (Mackintosh, 1960) and Kott (1969) mentions five ascidians as circumpolar, although others appear to be more localized. The South Georgian province, as defined by Kott, contains a mixed fauna, and she named six ascidian species which extend southwards into it from the Subantarctic. Material collected by the " Discovery " from South Georgia proper contained 15 species also known Zrom adjacent Subantarctic areas, out of a total of 32 species

THE BIOLOGY OF ASCIDIANS

66

(Millar, 1960). The faunistic relationship between South Georgia and the Magellanic and Falklaiid Islands area of the Subantarctic is also confirmed by the results of the Norwegian Antarctic Expeditions of 1928-30 (Millar, 1968). The mixed nature of the South Georgian fauna corresponds to a temperature regime intermediate between the Antarctic and cold temperate (Knox, 1960). As a whole the Antarctic has a large endemic element (Kott, 1969). A comparison has sometimes been drawn between the richness in species of the Antarctic and the relative poverty of the Arctic (Ekman, 1953). This contrast is not borne out by the ascidians, which havc about as many known species in the north as in the south polar areas ;it is not likely that a very unequal collecting effort is responsible for this result, because the ascidians of both regions have been described from most of the major expeditions. Kott (1969) speculated on the characteristics of the ascidian fauna of the Antarctic and Subantarctic. She concluded that viviparity is especially common, as shown by the prevalence of the Molgulidae, Agnesiidae and Polyzoinae. The evidence is rather slight since for instance only a few of the southern molgulids have been proved to be viviparous, although the disposition of the oviducts sometimes suggests that the eggs may be retained. Moreover the Polyzoinae are widely distributed in temperate and warm waters and their viviparous habit seems to be unrelated to polar conditions. Longevity and the large size of individuals or coIonies are frequent characters (Millar, 1960 ; Kott, 1969) and may be related to the richness of phytoplankton as well as to low temperature. Protective siphonal closing mechanisms are also mentioned by Kott, but it is doubtful whether they are particularly frequent in Antarctic ascidians, and indeed their relevance to Antarctic conditions is not clear. Kott also considered tho fauna to have many primitive elements, the families Agnesiidae and Corellidae being cited. The former has few species and is certainly well represented in south polar seas, but the Corellidae, with the possible exception of abyssal species, are as well represented in other areas. There is, too, little reason to regard the Corellidae or Agnesiidae as more primitive than the Ascidiidae, which has few Antarctic species.

Antiboreal Between the Antarctic Convergence and the Anti-boreal Convergence (or Subtropical Convergence) is an extensive area, containing a number of small isolated islands. I n addition, the south-eastern and south-western coasts of South America and thc South Island of New

66

R. H . MILLAR

Zealand lie within the same region, although the tempcrature regimes are not identical.

Antiboreal South America The ascidian fauna of the Patagonian Shelf, Magellan area and Falkland Islands is by now fairly well known mainly as the result of work by Herdman (1882, 1886), Michaelsen (1900, 1007), h n b a c k (1938, I050), Van Name (1945), Millar (1960) and Kott (1969). I

1 1 -4 I

I

I

I

,

I

I

I

I

I

Fic. 23. Distribution of A, Aplidium fuegiense ; B,StyeZa pnesderi; C, Polyoa opuntia; D, Alloeocnrpa iricruaiana ; E, Pyura legumen ; F, Paramolgula gregaria.

estimate that there are about 37 ascidian species in this fauna. The strongest affinity is with the fauna of South Georgia, as demonstrated by the ‘‘ Discovery ” collections in which 15 out of 24 species are also known from that island (Miller, 1960). The following species are either exclusively or mainly found in the area and may be taken as characteristic of its ascidian fauna : Aplidium fuegiense Cunningham, Styela paessleri Michaelsen, Polyzoa opuntia Lesson, Alloeocarpa incrustam (Herdman), Pyura legumen (Lesson) and Paramolgula pegaria (Lesson) (Fig. 23).

THE BIOLOGY OE ASCIDIANS

67

Antiboreal (Subanlarctic)islands

A number of islands in the Southern Ocean are of particular interest since they are subject to approximately the same water temperatures but are separated by great distances and sometimes by very deep water. Kott ( 1969) recognizes a Kerguelen province encompassing Kerguelen, Heard and Macquarie Islands. Although a number of species are apparently endemic to Kerguelen Island, others occur also at Macquarie Island some 90' of longitude to the east. She concludes that, despite its relative nearness to Campbell and Auckland Islands, Macquarie has more affinity to Kerguelen than to these islands, and only one ascidian species, Molgula sluiteri (Michaelsen), extends from the South Island of New Zealand and Chatham Island to Macquarie Island. The ascidians of Campbell and Auckland Islands are known mainly from the studies of Bovien (1921)) Michaelsen (1922, 1924) and Brewin (1950~~).Of the few species recorded, Didemnum studeri Hartmcyer, Corella eumyota Traustedt and Polyzoa reticulata (Herdman) are characteristically Subantarctic, and the islands appear to have been populated from that region rather than from nearby New Zealand, despite the contrary conclusion by Kott (1969). If this is true, the ascidians conform to the faunistic pattern of the molluscs (Hedley, 1916) rather than of the sponges and echinoderms (Ekman, 1953). The Chatham Islands and the relatively shallow Chatham Rise connecting them to the South Island of New Zealand have an ascidian fauna described by Sluiter (1900), Michaelsen (1922, 1924) and Brewin (1956b). Brewin showed it to have a close alliance with the ascidian fauna of New Zealand, 21 of the 33 Chatham species being known from there. No distinctly southern element is present, in contrast to the situation in the Campbell and Auckland Islands. The Chatham Islands lie farther north and, unlike the Campbell and Auckland Islands are subject to warm northern water in addition to cool southern water. The Tristan da Cunha group, like the Chatham Islands, lies near thc Antiboreal Convergence. Occupying a very isolated position between South Africa and South America, these islands appear to have an ascidian fauna, so far as can be judged from the very scanty records, which has some affinity with that of southern South America but none with the South African fauna (Millar, 1967). N e w Zealand Knox (19GO) recognized the Aupourian, Cookian and Forsterian provinces, and my estimates of respectively about 81, 35 and 58 ascidian species are based for the most part on a series of papers by

68

R. H. MILLAR

Brewin (1946, 1948, l950b, 105Oc, 1950d, 1051, 1952a, 1952b, 1954, 1957, 1958a, 1958b, 1960). In some cases it is possible to recognize closely related species with allopatric distribution, as Pyura pachydermatina (Herdman) from the South Island, P . spinosissima Michaelsen from the North Island, and P . chathamensis Brewin from the Chatham Islands (Brewin, 1952b ; Knox, 1063). Distributions of this kind may have resulted from past fluctuations in the position of the boundary between the warm and cold watcr masscs, for which geological evidence exists (Knox, 1963). Other regions of the sea rich in species may also have been subject to such changcs in hydrographic boundaries which promotc speciation.

South Africa The coastal and off-shore waters of South Africa, like those of New Zealand, are influenced by the proximity of warm and cool currents. On the east coast the fauna is tropical at least as far south as Durban, but the south coast from about Algoa Bay to Cape Point supports a distinct fauna. The third faunistic division is the Namaqua fauna, occupying the coast from Cape Point to 18"s and is subject to the cool Benguela Current and to the upwelling of cold deep water. South African ascidians have been extensively studied, by Hartmeyer (1911, 1912, 1913), Michaelsen (1904, 1915, 1923, 1934) and Millar (1955a, 1962b, 1964a), and some 84 species may be recognized, according t o my estimate. A large and representative collection amounting to 69 species taken from coastal waters between Morrumbene on the tropical east coast and Saldanha Bay in the southern part of the Namaqua area showed 39% warm-water, 22% cold-watcr, 4% ubiquitous and 35% south-coast components (Milhr, 1062b). These figures are in quite good agreement with those of Stephenson (1944) for littoral animals as a whole. About half of the South African ascidians are endemic, and the general affinities of this fauna are with the adjacent areas of the warmer Indian Ocean. There is, however, evidence of some relationship with the Antiboreal fauna, in the presence of Aplidium retiforme (Herdman) which also occurs at Kerguelen, Corella eumyota Traustedt, which is widely distributed in southern waters, and Agnesia glaciata Michaelsen (Millar, 1962b). The endemic Sycozoa arborescem Hartmeyer marks the occurrence of a genus characteristic of the Antarctic, Subantarctic and western Pacific. One may conclude that, in the main, the South African ascidian fauna has bcen derived from the Indo-west-Pacific but that a small element originated from the Antiboreal, possibly in a geological period when the Antiboreal Convergence lay farther north than at present.

THE BIOLOGY O F ASCIDJANS

69

Tho ascidians of othcr parts of the world havc been so little investigated or the studies havc bccii so spccializcd-as tho taxonomic rcview of tho Dideninidan: of tlic lndo-Pncific (Eldredgc, 1967)-that general spcculation 011 their faunistic relationships is unprofitable. B. Deepwater aseidium

A number of vertical zones have been recognized in the deep water beyond the shelf, but the terminology and limits applied to them have varied considerably (Hedgpeth, 1957 ; Vinogradova, 1962b). Vinogradova (1969a)recognized a bathyal zone from 500-3 000 m mainly on the slope, an abyssal zone from 3 000-6 000 m constituting most of the sea-floor, and an ultra-abyssal zone in depths greater than 6 000 m and corresponding t o the hadal zone of Bruun (1956). The upper limit of the abyssal zone is somewhat arbitrary, and Ekman (1953) has emphasized that it is not the same in all parts of the oceans. Many abyssal species certainly extend up to 2 000 m and this is the depth which I am taking as the upper boundary. Whether the floor below 6 000 m supports a distinctive fauna is not certain. According to Wolff (1960) it does, but Menzies and George (1967) believe that there is little evidence supporting the view. Very few ascidians have been found at such depths, although they do occur down to 8 430 m in the Kuril-Kamchatka Trench (Vinogradova, 1969a, b, 1970). In less extreme depths there exists a moderately rich ascidian fauna representing several families (Table IV, below). This fauna is known mainly from the accounts of Herdman (1882, 1886, 1888), Verrill (1885), Ritter (1907), Sluiter (1904),Hartmeyer (1911,1912),Michaelsen (1904),Millar (1955b, 1959a, 1964b), Monniot and Monniot (1968) and Kott (1969), whose records are incorporated in Fig. 24. In addition to the bathymetric divisions, geographical divisions are also to be recognized in the abyssal parts of the sea. Ekman (1953) broadly divided the deep seas into the Atlantic, Indo-Pan-Pacific, Antarctic, Arctic, Mediterranean, Red Sea and Sea of Japan. Following a review of subsequent faunistic studies, Vinogradova (1956, 1962b) proposed thc scheme used in Fig. 24, which recognizes more subdivisions. The validity of the geographical areas depends on the distinctness of their faunas, and there is some evidence that the abyssal faunas of the oceans show a measure of independence from one another. Vinogradova (1962b) concluded that, for a number of invertebrate groups taken as a whole, the proportion of endemic species in the Atlantic Ocean is 76%, in the Pacific Ocean 73.2% and in the Indian Ocean slightly over 50%.

60

40

20

0 20

40

60

90

60

30W.

0

30.5.

60

90

I20

150

180

150

120

90

FIG.24. Records of ascidians from water deeper 'than 2 000 m. Zoogeographical divisions : A, Pacific-North-Indian area ; A( 1)Pacific sub-area ; A( la) North Pacific Province ; A( Ib) West Pacific Province ;A( Ic) East Pacific Province ;A(2), North-Indian sub-area ; B, Atlantic area ;B(1) Arctic sub-area ;B(2) Atlantic sub-area; B(2a) North Atlantic Province ;B(2b) West Atlantic Province ; B(2c) East Atlentic Province ; C, Antarctic area; C(1) Antarctic-Atlantic sub-area; C(2) Antarctic-Indian-PacSc sub-area; C(2a) Indian Province; C(2b) Pacific Province.

TABLE IV ASCIDIANS FROM DEPTHS GREATERTHAN 2 000 M Speciea Family Clavelinidac ? Podoclavella sp. Distaplia galathem Millar Hypsistozoa obscura Kott Protoholoroa pedunculata Kott Polycitor fungiforinis Millnr ? Eudhtorna vitreum (Sars) Family Polyclinidae Aplidiuna abyssuna Kott Synoicurn tentaculaluna Kott Pharyngodictyon inirabile Herdman Family Didemnidae Leptoclinulea faeroensis Bj erkan Family Corellidae ? Chelyoeoma inaequale Redl korzev Abyssascidia rcycillii Herdman Corynaeculia su hmi Herdman Corellopsis tranalucula Xllar Benthaecidia michaelseni Ritter

Localitiea

Depth (m)

Reference8

58'06's 44"55'\V 3G031'S 178'38'W 08"lO'S 81'08'W 55'54's 58"59'\\' ; 56'18's 37"04'\\' ; 57"04'S 70'59'W ; 64"Ol'S 67"44'W ; 65'37's 123"55'\V 48'34'5 36'04'W 55'37'X 56"08'\V

2800 4410 6006 2818-5000

Kott, 1969 Millar, 1959 Kott, 1969 Kott, 1969

5187-5251 2078

Millar, 1970 Millar, 1970

08"lO'S 8l008'\V 58"OG'S 44"55'\1: 46" 16's 48'27'E

6006 2800 2928

Kott, 1969 Iiott, 1969 Herdniaii, 18SG

37'25'N 73@06'\V

2895

Van Kame. 1916

07'21"

3638

Van Xamc, 1945

4680-5900

Herdman. 1882 ; Millar, 1959 Hartmeycr, 1911 ; 1912 ; 1923-24; Herdman. 1582 Millar. 1970 Rittcr, 1907

79"02'W

32'10's 175'54'W; 42'42's 131'10'E

58'01's 44"45'\\' ; 61'50'5 56@27'\\'; 33'31's 74'43'1V ; 433-5858 46'66's 45@31'E; 54"17'S 27"25'\\' ; 63"lG'S 57'5l'E 07"30'S 81"25'\\' 33"03'N 120"42'\\;

5857-5858 3927

TABLEIV-wntd ~

Species Family Hypobythiidae Hypobythiw calycodes Moseley ? Megalodicopia hkna Oka Family Agnesiidae Agnesia depessa Millar

A d a g e bi;jida Millar Family Ascidiidaa Bathyascidia VaBCuloaa (Herdman) Family Octacnemidae 0ota;cnernw bythiw Moseley Octacnemw, herdrnani Ritter Family Styelidae Styela sericata Herdman

Styela rnilleri Ritter Styela p d l a Herdman Styela sqmrnosa Herdman Styela bathybia (Bonnevie) Styela loculosa Monniot and Monniot

Lomlities

37'41"

177'4W

~~

Depth (m)

~

References

5220

Moseley, 1876

13'15'5 78'06W

5234-5314

Kott, 1969

24'12" 63'23W-24'28'N 63'18W; ?5'25'S 47'09%; ? 36'34'5 14'08'E 09'22" 89'33W; 07'35'5 81'24W

4820-5860

Millar, 1955; 1959

3517-5841

Millar, 1970

53'55's 108'35%

3510

Herdman, 1888

2'33% 144'04'E ; 36'23% 177'41%

1957-2640

5'17's 85'19W; 6'54'5 83'34W

40634087

Moseley, 1876; Millar, 1959 Ritter, 1906

24'12" 63'23W-24'28'N 63'18W; 5'32% 78'41'E ; 3510-5860 1'56" 77'05'E ; 3'23% 44'04'E ;5'25'5 47'09% ; 7'24'5 48'24% ; 25'11's 59'59% ; 36'31's 178'38W; 36'34'5 178'57W ; 39'45's 159'39% ;43'58'5 165'24% ; 45"51'S 164'32% ; 53'55's 108'35%; 68"03'S 130'46W 33'01" 121'32W; 9'23" 89'32W; 1'42" 7'51%; 3281-4077 06'21T 80'41W; 10'15's 95'41W 36'10'N 42'42'5 75'12" 57'50'N

178"O'E 134'10'E 3'20% 54'06W; 38'16"

71'47W

3751 4758 2195 2864-3369

Herdman, 1888 ; Kott, 1969 ; Millar, 1955; 1959; 1970

Millar, 1959; 1969; Ritter, 1906; Van Name, 1945 Herdman, 1886 Herdman, 1882 Bonnevie, 1896 Monniot and Monniot, 1968; Millar, 1970

Family Styelidae

Minostyela clavata K o t t ? Styela nordenakjoldi Michaelsen Styela sp.? Cnemidocarpa bythia (Herdman) Cnemidocarpa bathyphila Millar Cnemidocarpa bifurcata Millar Cnemidocarpa peruviana Millar Cnemidocarpa digonaa Monniot a n d Monniot ? Cnernidocarpa drygalskii (Hartmeyer) Cnemidocarpa sp. Polycarpa albatrossi (Van Name)

Polycarpa pseudoalbatrossi Monniot and Monniot Dicarpa simplex Millar Dicarpa paci$ca Millar Bathyoncuo diacoideua Herdman Bathyoncuo herdmani Michaelsen Bathyoncuo minutus Herdman Bathyoncua mirabilia Herdman

58"18'S 16Oo03'W 13'15'5 78'06'W

3587-3817 5234-5314

Kott, 1969 Kott, 1969

59'57'5 32'09'5 42'42'5 01'03'N

136'37'W 3386-3477 176'35'W; 32'10'5 177'14'W; 32'10'5 175'54'W; 4400-7000 134'10'E ; 43'58'5 165'24'E ;45'51'5 164'32'E 18"40'W-00"58'N 18'37'W 5250-5300

Kott, 1969 Herdman, 1882 ; Millar, 1959 Millar, 1955

9'23"

89"32'W

3570

Millar, 1964

3369-5760

Millar, 1970 Monniot and Monniot, 1968 Van Name, 1945

07'32'5 81'26'W; ? 57'50"

54'06'W

38'46"

70'06'W

2886

06'21"

SO"41'W

3281

9'23" 89'32'W 39'26" 70'33'W 38'30" 69'08'W 37'38" 73'16'W 9'49'5 114'13'E 39'26" 70'33'W 40'33" 9'23" 9'25" 9'15" 35'41"

; 39'05" ; 38'24" ; 5'32" ; 38'46"

3570 70'44'W ; 38'46" 7O"OG'W ; 2598-4350 71'52'W; 38'22" 70'17'W; 78'41'E ; 1'56" 77'05'E ; 70'06'W

2496-2886

35"24'W-40°34'N 35'52'W ; 36'38'5 178'21'W ; 2470-4600 89'32'W 3514-4050 89'22'W ; 9'24" 89"27'W; ? 9'22" 89'33'W; 89'29'W; 9'23" 89'32'W ; 6'08's 82'41'W 157'42'E 4209

Millar, 1959 Millar, 1969 ; Monniot and Monniot, 1968; Van Name, 1945 Monniot and Monniot, 1968 Millar, 1955; 1959 Millar, 1964; 1969; 1970 Herdman, 1886

63'16's 57'51'E

4636

Michaelsen, 1904

38'09"

5718

Herdman, 1886

2928

Herdman, 1882

156'25'W

46'16'5 48'27'E

TABLEI V - e o n t d Localities

Species Family Styelidae Bathyst yeloides enderbyanus (Michaelsen)

Hemistyela pilosa Millar Kuekenthalia borealis (Gottschaldt) Family Pyuridae Bathypera splendens Michaelsen Pungulus antarcticus Herdman Pungulus cinerew Herdman

Depth (m)

References

3'54" 8'22'W; 1'42" 7"51'E ; 1'03" 18"40'W0'58" 18'37'W; O"42'N 5"59'W ; 3'23's 44'04'E ; 4"OO'S 8"25'E ; 4"47'S 46'19'E ; 5'25% 47'09'E ; 29'42's 33'19'E ; 40"lO'S 6"05W; 45'47% 164'39'E ; 45"51'S 164'32'E ; 63'16's 57"51'E l"03" 18"40'W-0°58'N 18"37'W 55"37'N 56'08'W

2550-5300

Michaelsen, 1904 ; Millar, 1955; 1959

5250-5300 2078

Millar, 1955 Millar, 1970

63'16% 57'51'E

350-4636

Michaelsen, 1904

46'46's 45'31'E ; 64'48's 44'26'W

2928-4548

Herdman. 1912

Culeolua murrayi Herdman

46"16'S 58'06's 35'41" 62'03's 65'37'5

48'27'E; 55"52'S 24'49'W; 55"54'S 58"59W; 2818-5918 59'27'W; 64'01's 67"44'W 157'42'E ; 55'01's 44'20'W; 55'54's 58'59'W; 2818-6207 129"38'W; 62'39'5 64"02'W; 64'01's 67'44'W; 121"06'W; 65'37'5 123"55'W; 66"ll'S 102"28'W

Culeolus moseleyi Herdman Culeolus pyramidalis Ritter

O"33'S 151"34'W 33'01" 121"32'W ; 32'54"

121°15'W; 9'23"

89'32'W

Culeolus recumbens Herdman 46'46'5 45"31% 13'26" 145"40'E Culeolua inversus Oka 47'26" 07'53'W ; 40'33" 35'24'W-4Oo34'N 35"52'W ; Culeolus suhmi Herdman 39'22" 68'25W; 37'25% 71'40'W; 5'32" 78"41'E ; 3'38" 78'15'E 3"23'S 44'04'E ; 5'25% 47'09'E ; 14'20's 45"09'E ; 44'18's 166"46'E ; 44"33'S 49'19'W 62"54'S 118'52'E 4e016'S d S D 2 7 ' E

3800

Herdman, 1882 ; Kott, 1969 Hartmeyer, 1911 ; 1912; Herdman, 1882 ; Michaelsen, 1904; Kott, 1969; Vinogradova, 1970 Herdman, 1882 Ritter, 1907 ; Van Name, 1945 Herdman, 1882 Oka, 1928 Herdman, 1882 ; Kott, 1969 ; Millar. 1955; 1959; 1969; Van Name, 1945 Vinogradova. 1962

2986

Hnrdrnnn

4438 3570-4066 2475-3594 3500 2894-5329

. 1852

Family Pyuridae Culeolua uachakovi Redi korzev Culeolics willemoesi Herdman Culeolus parvus Millar Eupera chuni Michaelsen ? Heteroetigma singulare (Van Name) Family Molgiilidae Molgula bathybia (Hart meyer) Afolgula verrilli (Van Name) illolgulu galatheae Millar ilfolgula sp. dfolgula (.Volguloides) imtnziizda (Hartmeyer)

3lolgctla (.llolgtcZoules) sphaeroidea Millar Family Hesacrobylidac Hexucrobylus indicus Oka

46'41.5"

3500

Redikorzev, 1941

4209 3500-4893 4990 5005

Herdman, 1886 Millar, 1969 ; 1970 Michaelsen, 1904 H a r a n t , 1929

63'16's 57"Bl'E

4636

H a r t meyer, 1912

40'29" 66"04'\\' 1 ' 4 2 3 7'5l'E ; 0'42" 5'59'\V 36'34's 14'08'E: 3"56'S 118"26'E ; 20'29's 103"26'JV ; 32'03's 72"40'\V GO"57'S 5G052'\V

3237 2550-5160 4893 1788-5929

7'35'8 8i024'\V; 10'13's 80"05'L\..

5825-6328

Van S a m e , 1912 Millar, 1959 JIillar, 1970 K o t t , 1969 ; 3Iilltir, 1959; 19G9; Van S a m e , 1945 Millar, 1970

39"26'S 70"33'\\' ; lO"07'S 89'50'\V ; 5'325 58"41'E ; l"j(j'N 77'05'E ; 8"52'5 49'25'3

891-5020

3.5'41" 36'34's 2"56'N 38'54"

147O28'E 157'42'E 14'08'E ; ? 56'37's 34'48'W 1l"4O'W 21'06'W; 36'54's 2OC46'\V

Hexacrobylics paanantatodes 45'5 1'S 164"32'E Sluiter Oligotrema psatnmites Bourne 60'57% 56"51'\V Oligotrema sp. 8"lO'S 81"08'\V Gmterascuiia sandersi 36'23" 67"58'\V ; ? 45~~34'3 Gc02'E Monniot antl Monniot

4400 2672-3020 6006 4618-4680

K o t t , 1969 ; llillar, 1959; 1969; 1970; O h , 1913 Jlillar, 1969 Boiirnr. 1903 Kott. 1969 3Ionniot a n d Jlonniot , 1968

Vinogradora (1969b, 1970) has recorded the following species from the Kuril-Kamchatka Trench: Sif ttlrr pellirrtloarc Vinogratlova, c. robusfus \'ino&radova, C'. murrnyi Herdman, C . longipeduculolua Vinogratlova antl Ponreztleolcta bicristntus Vinogratlova. Citleolua Icnuia Wnogradova,

8

s s 8

s E 0

m

0 ul

m

0

0

4 0 ul

8 0 ul

*

o

N

o

o

g

o 0

0 ul

THE BIOLOGY OF ASCLDIANS

77

My own estimates for the ascidian species, based on the published records, are: Atlantic Ocean 72%, Pacific Ocean 68% and Indian Ocean 43% (Millar, 1970), and the group appears to support the view that abyssal faunas show zoogeographical divisions. Certain features of the ascidians, however, such as the plasticity of body form, seasonal changes in structure, and a high degree of variability, have led to uncertainty in the recognition of species, well illustrated by the synonymy proposed by Kott (1969) for Cnemidocarpa nordenskjoldi and for Culeolusmurrayi Herdman. I n the presence of such uncertainties, which are common in abyssal species where identification often rests on few specimens, reliable conclusions on specific endemism are difficult to reach, and it may be useful to consider small distinctive genera, and pairs or groups of similar species whether or not these ultimately prove to represent a single species. By choosing taxa with highly unusual characters-and these are frequent in abyssal forms-we may be confident that we are not dealing with species merely having a similar appearance through adaptive convergence. Styela loculosa Monniot and Monniot and Minostyela clavata Kott, which are characterized by a peculiar form of gonad quite unlike that of any other known ascidian, show a kind of bipolar distribution (Fig. 25). Another group of highly aberrant abyssal ascidians comprises Hexacrobylus indicus Oka (synonym H . arcticus Hartmeyer) and H . psammutodes Sluiter (Fig. 26). Oligotremapsammites Bourne is evidently of the same group of species, but is known only from a depth of 92 m. Kott (1969) believed that all of these represent one species, and although I do not accept this opinion in view of the structural differences in the pharynx, oral tentacles and gut, there is no doubt that the species form a closely related group with a marked systematic separation from other ascidians. The distribution is wide (Fig. 26) and cuts across the boundaries of several regions. The genus Culeolus presents another interesting case, and whether or not Kott (1969) is right in taking 11 of the described species as synonyms of C. murrayi Herdman the great difficulty in separating species underlines the advantage of grouping all together for the present purpose. The wide distribution (Fig. 26) lacks records principally in the Indian Ocean and north polar seas. The last example is the genus Corynascidia (Fig. 25). C . suhmi Herdman is known from widely separated areas and although not recorded from low northern or southern latitudes, it may be expected to occur in most of the deep oceans (Kott, 1969). As known at present its distribution suggests some degree of bipolarity. C. sedem Sluiter and C . herdmuni Ritter have been taken in depths less than 2 000 m from Indonesia and the North Pacific respectively.

FIQ.26. Known distribution ofHezacrobylua indicua ( 0 ) Hexacrobylua . indicuo < 2OOOrn (a), Hexacrobylua paammalodee ( 0 ) .culwlua spp. (a), Bothyetyeloides enderbyanuo (*).

THE BIOLOQY OF ASCIDIANS

79

If we can rely on these few cases where it is reasonably sure that we are dealing with one species or at most a few closely related species, there is less evidence t o support the view that abyssal ascidians conform to the zoogeographic divisions proposed by Ekman and by Vinogradova. Rather they appear t o be widely distributed in the abyssal regions and a t most tend t o have either an equatorial distribution or t o occur in higher latitudes of both the northern and southern hemispheres. There is therefore conflict between these conclusions based on the one hand on all recorded species and on the other on aberrant or very distinctive species. Only if these groups of distinctive ascidians proved t o consist of separate, although similar, species, would the contradiction be removed, with the conclusion that a considerable degree of specific endemism exists. The distribution of abyssal ascidians as a whole is by no mcanR uniform, even within a single region, as Sokolska (1969) shows for the Pacific Ocean. An analysis of all occurrences in the abyssal Pacific recorded by the main deep-sea expeditions shows the ascidians t o be much more restricted than, for example sponges, which might be expected t o have rather similar requirements. IMPORTANCE VIII. ECONOMIC A. Fouling In comparison with some other groups of marine animals thc ascidians cannot be said to have great economic importance. As fouling organisms, however, they are significant and contribute largely t o the problem of growth on the hulls of ships, on buoys and floating structures and on fixed harbour installations. The list of over 100 ascidian species in “ Marine Fouling and its Prevention ” (Woods Hole Oceanographic Institute, 1952) indicates their potential importance, although many of the species recorded are not sufficiently abundant t o be harmful. Almost any shallow-water species in which the adult is normally attached to a firm substratum may appear in a fouling community. Ascidians have been studied as they occur on ships’ hulls (Berner, 1944 ; Skerman, 1960), but more often workers have used test panels or blocks which are examined periodically t o follow the course of fouling (Weiss, 1948 ; Sentz-Braconnot, 1966 ; Relini, 1964 ; Stubbings and Houghton, 1964 ;Allen and Wood, 195.0 ; Elroi and Komarovsky, 1961 ; Kawahara, 1962; Nair, 1962 ; Raja, 1963 ; Skernian, 1959). Whatever methods of asscssment are used, it is evident that ascidians form a major part of the fouling community in many regions of the world. Of

80

R. 11. MILLAR

about 22 ascidian species listed in a report on marine fouling (Organization for Economic Co-operation and Development, 1966), four were classed as principal fouling species, and a number of workers have noted the group as contributing the dominant fouling organisms (Relini, 1964; Stubbings and Houghton, 1964 ; Berner, 1944; Scheer, 1945; Weiss, 1948; Skerman, 1959; Kawahara, 1962). Often they are not prominent in the early stages of the development of a sessile community, but become the principal organisms in later stages. Thus Berner (1944) found that on ships’ hulls at Marseilles there was a regular succession, from Enteromorpha, through Bryozoa and sessile annelids to barnacles and Ciona intestinulis. In Kingston Harbour, Jamaica the primary colonizers were algae and barnacles, but the ascidians Didemnum conchyliatum (Sluiter) and Ascidia nigra became and remained dominant for many months (Goodbody, 1963b). The sequence, and the species involved, naturally vary with the location, and in California, U.S.A., six stages in fouling were recognized, one of which was dominated by an almost pure growth of Cionu, which was subsequently replaced by mussels and barnacles (Scheer, 1945). At Auckland, New Zealand, the initial settlers were barnacles and hydroids but these subsequently gave way to oysters and the ascidian Microcosmus kura Brewin (Skerman, 1959). Similarly in Japanese waters, Styelaplicata became one of the two dominant species in the later stages of fouling (Kawahara, 1962). The relative importance of ascidians depends on the season at which surfaces are exposed to fouling, and ReIini (1964) found that at Genoa, Italy, they were most abundant on test panels in winter, but varied considerably in abundance from year to year. This was also the experience of Elroi and Komarovsky (1961) with Ciona at Haifa, Israel, and of Stubbings and Houghton (1964) during their study of Chichester Harbour, England, where Diplosoma Zisterianum gradually declined in numbers over a period of several years. Some idea of the importance which ascidians may have in the fouling of vessels is given by the numbers recorded by Elroi and Komarovsky (1961), who estimated 2 500-10 000 specimens of Cionu per m2 of exposed plate ; the individuals reach a length of 25 cm, and the total wet weight on 1 m2 was 140 kg. Under favourable conditions Ascidiella aspersa may settle a t the rate of 1 800/m2 per day (Millar, 1961b). It is not so much the weight of the animals which creates a problem, for their under-water weight is not great, but the additional friction which they cause to a moving ship. This must vary in a complex way with the size, shape and roughness of the body, but has not been studied. On floats and other stationary objects ascidians are

THE BIOLOGY OF ASCTDTANS

81

troublesome mainly because they have to be removed when the structures are painted. The settlement and growth of ascidians m;iy also bc a problcin in fisheries. In oyster culture, for example, they often smother surfaces intended for the settlement of the molluscan larvae, impede dredging, or contribute to the silting of oyster beds (Cole, 195G; Waugh, 1957; Millar, 1961b ; Hancock, 1969). Some degree of control can be achieved by treating the settlement surfaces with chemicals (Loosanoff, 1960; Waugh, 1957). Accidental transport is a conscquence of fouling, and has accounted for the introduction of Styela clava to the south coast of England, probably from Korean waters (Carlisle, 1954b ; Houghton and Millar, 1960). The species has subsequently multiplied and spread t o the extent that it is now the dominant large ascidian in certain sheltered coastal waters. It is probable that the widespread occurrence of Ciona intestinulis and Diplosomu listerianum in the harbours of many countries is likewisc the result of introductions on ships’ hulls. Certain structural and biological characters help to cxplain why ascidians are important as fouling organisms. Firstly, because the branchial cavity is large, the total volume and surface area of an individual are high in relation to the tissue weight, and an ascidian therefore occupies a large space or covers a large area. Secondly, being efficient filter-feeders, they grow fast and can outpace many of their competitors. Larval behaviour, too, pre-adapts them as fouling animals, since the larvae initially swim upwards, reaching the surface layers of water where they encounter floats and ships’ hulls, to which they attach themselves. Moreover, the short pelagic life of the larva favours heavy settlenient near the parents, and in harbours there is generally a stock of adults. Some species, in addition, are resistant to reduced salinity or to pollution (Huus, 1933; Berner, 1944; SentzBraconnot, 19GG; Dybern, 1967, 196%; Diehl, 1957; Van Name, 1945; Gunter and Hall, 1963; Dragovich and Kelly, 1964), and these are conditions met in harbours, where fouling on ships is a problem.

B. Food of man, and of commercial fish In some countries, mainly those of the far East and certain parts of the Mediterranean, ascidians are eaten by man and are sufficiently important to merit an entry in the F.A.O. Yearbook of Fishery Statistics (Food and Agriculture Organization, 1964). Microcosmus sulcatus, and occasionally Styela plicata and Polycarpa pomuria are taken in the Mediterranean (Harant, 1951),Halocynthia roretzi in Japan, where it is cultured in the north of Honsyu (Tokioka, 1953), and Pyura chilensis

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in South America (Van Name, 1945). Margalino and de Stefan0 (1960) found that the flesh of Microcosmus sulcutus is almost as digestible as whole egg, and the protein content higher. Such is their abundance in some localities that ascidinns have been considered as a possible source of cellulose, vanadium, protein and other chemicals (Elroi and Komarovsky, 1961 ; Hebant-Joder, 1965), and although the investigations have been confined to warm waters they might encourage a similar approach applied to some of the dense and fast-growing populations encountered in certain temperate areas. The part played by ascidians in the diet of commercial fish, and their occasional use as bait, have been mentioned elsewhere (p. 48).

C . Uptake of harntful substances Since the advent of nuclear weapons and nuclear power stations the presence of radionuclides in the sea and their uptake by marine organisms have received considerable attention. So far as ascidians are concerned the practical importance of the uptake of radioactive materials is the possibility that they will be concentrated in the tissues and passed on to man, either when ascidians are eaten or indirectly through the consumption of commercial fish which themselves feed on the ascidians. According to Bryan (1963) Ciona intestinalis shows a low concentration factor for 13'Cs in all tissues, and Strohal et al. (1969) found factors of 70 and 90 for Phallusia mammillata and Microcosmus sulcatus. go,, is of particular importance as an artificial radionuclide, but factors of only 1 and 4 were obtained by Strohal et al. for P . mammillata and M . sulcatus. These workers found Zn t o be eoncentrated by a factor of 940 in both species, although Ciona intestinalis has a factor of 6 600 (Vinogradov, 1953). Co and Fe are also of interest as pollutants, and 1Microcosmus sulcutus has factors of 1 350 and 40 000 respectively, the corresponding factors for Phallusia mammillata being 400 and 18 000 (Strohal et al., 1969), and for Ciona intestinalis, 400 and 200 respectively. It is evident that there may be some danger, in certain areas of the sea subject to radioactive pollution, of radionuclides passing up the food chain to man. IX. REFERENCES Abbott, D. P. (1951). Boatricliobranchue digonaa, a new molgulid ascidian from Florida. J . Waah. A d . Sci. 41 (9), 302-307. Abbott, D. P. (1953). Asexual rcproduction in the colonial mcidian M e t u ? m carpa taylori Huntsman. Univ. Calif. Piibb 2001.61 ( l ) , 1-47. Abbott, D. P. (1955). Larval structuro and activity in tho aacidinn Melandrocurpa taylori. J . Morph. 97,569-594.

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Bell, L. G.E. (1955). Effect of chlorctone on tunicatc cmbryos. Nature, Lond. 175, 1048.

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Adv. mar. Biol., Vol.

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PLANKTON AS A FACTOR IN THE NITROGEN AND PHOSPHORUS CYCLES IN THE SEA E. D. S. CORNERand ANTHONY G. DAVIES Marine Biological Association of the United Kingdmn, The Laboratory, Citadel Hill, Plymouth, England I. Introduction . . .. .. .. .. .. .. .. .. 11. The Chemical Forms of Nitrogen and Phosphorus Dissolved in Sea Wator A. Inorganic Nitrogen . . .. .. .. B. Physico-chemical Roactions .. .. .. .. .. C. Organic Nitrogen .. D. Inorganic Phosphorus .. .. .. .. E. Organic Phosphorus .. .. .. .. 111. The Stoichiomctry of Biologically Induced Changes in Nutrient Levels . A. The " Assimilation Ratio ", AN :AP . .. .. .. B. Apparent Oxygen Utilization . .. IV. Uptake of Nitrogen Compounds by Phytoplankton. . .. .. .. A. Inorganic Forms of Nitrogen . .. .. .. * . B. The Effect of Light . . .. .. .. .. . . .. C. The Hyperbolic Relationship .. .. .. V. Uptake of Phosphorus Compounds by Phytoplankton .. A. Inorganic Forms of Phosphorus .. .. B. Organic Forms of Phosphorus . .. .. .. VI. The Effect of Nutrient Levols on Phytoplankton Growth Kinetics . VII. Nitrogen and Phosphorus Levels in Phytoplankton .. .. .. Release of Organic Forms of Nitrogen and Phosphorus by PhytoA. plankton ,. .. .. .. .. .. .. VIII. The Assimilation of Nitrogen and Phosphorus by Zooplankton . .. A. Living Diets . . .. .. .. .. .. .. B. Detritus .. .. .. .. .. .. C. Dissolved Organic Matorial .. .. .. .. D. Laboratory Studies on Assimilation .. E. Superfluous Feeding . .. .. .. .. IX. Levels of Nitrogen and Phosphorus in Zooplankton . . .. .. X. Nitrogcn and Phosphorus Excretion by Zooplankton .. .. A. Nitrogcn Excretion . . .. .. .. .. .. B. Phosphorus Excretion . . . . .. .. .. .. C. Seasonal Surveys of Nitrogen and Phosphorus Excretion .. D. Nutrient Regeneration .. .. .. .. .. XI. Growth of Zooplankton in Terms of Nitrogen and Phosphorus . . A. RateofGrowth .. .. .. .. .. .. B. Egg Production ... ... ... ... ... C. Net and Gross Growth Efficiencies .. .. ..

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I. INTRODUCTION This review is primarily concerned with quantitative aspects of the relationship between organically-boundforms of nitrogen and phosphorus in Suspended material in the sea, and the inorganic forms of these elements dissolved in sea water. In dealing with suspended material we have concentrated almost exclusively on planktonic organisms: since, although a large proportion may be present in the sea as detritus, this fraction has recently been considered in a review in the present series (Riley, 1970); moreover, another recent review (Johannes, 1968) has absolved us from the need to deal in detail with the role of bacteria. A further limitation to our treatment has been imposed by the fact that research on topics such as the chemistry of nutrients in sea water has continued for well over half a century and has given rise to a vast and scattered literature : accordingly, while we have occasionally given detailed consideration to earlier studies that have, in our view, been particularly valuable, we have tended for the most part to concentrate on more recent publications, namely those appearing in the last ten years or so. Again, for reasons less valid but perhaps understandable, some degree of bias in our selection of topics may have resulted from our own research interests. Our general approach has been to deal with the nitrogen and phosphorus cycles in the sea in terms of (1) the sea water-phytoplankton relationship (2) the phytoplankton-zooplankton relationship and (3) the zooplankton-sea water relationship. In addition, as many of the studies considered under these headings have involved laboratory experiments using plants and animals confined in small volumes of sea water, we have extended our treatment to include a final section dealing with field observations that illustrate the interrelationships of plankton and nutrient levels in the open sea.

11. THECHEMICALFORMS OF NITROGEN AND PHOSPHORUS DISSOLVED IN SEAWATER Throughout this review, we shall frequently refer to nitrate and phosphate as important nutrients for phytoplankton growth. However, the sea contains several other dissolved forms of nitrogen and phos-

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phorus, some of which may aIso be utilized by the plants. Accordingly, before dealing with iiutricnt assimilation by phytoplankton, wc give here a brief account of the various chemical forms of dissolved nitrogen and phosphorus prescnt in the sea. A. Inorganic nitrogen The molecular gas, N2, is the predominant form of nitrogen in the aea. Its solubility was measured by Rakestraw and Emmel (1938) and their data indicate that at lO"C, sea water of salinity 35%, in equilibrium with the atmosphere would contain about 500 pg-molell. The extent to which this form of nitrogen is involved in the marine biocycle is somewhat uncertain. Benson and Parker (1961), who examined nitrogen : argon ratios in the Atlantic Ocean, found that, within a 1% experimental error, the measured ratios agreed with that expected from dissolved air. They concluded that molecular nitrogen is not utilized in the sea. Nitrogen-fixing organisms do, in fact, occur in certain marine environments (Allen, 1963); but the supply of dissolved carbohydrate available in the sea is probably insufficient to satisfy the high metabolic energy requirement of continuous heterotrophic fixation (Vaccaro, 1965). A more interesting possibility is that this energy may be provided by sunlight in a manner similar t o photosynthesis (Fogg and Than-Tun, 1958), and the finding that nitrogen-fixation by colonies of the blue-green alga Trichodesmium occurred only in the light (Dugdale et al., 1961) supports this idea. The main inorganic forms of fixed nitrogen in the sea are the ammonium cation-the equilibrium constants for the protonation of ammonia in solution (Sillen and Martell, 1964) indicate that at least 97% would be present as the ion-and the nitrate and nitrite anions, nitrate being the most highly oxidized form of nitrogen in the sea and the major source of the element available for use by phytoplankton. The concentrations of these ions vary considerably, both seasonally and geographically (see Section XII),but in general fall within the following ranges (Sverdrup et al., 1942): NHt-N, 0.35-3-5 pg-atoms/l; NO,-N, 0.01-3.5 pg-atomsll; and NO;-N, 0.1-43-0 pg-atomsll. Very low Concentrations of nitrous oxide, N,O, have been detected in the Atlantic and Pacific Oceans (Craig and Gordon, 1963), the levels being higher in the equatorial region, possibly due to the increased activity of denitrifying bacteria. The question of whether hydroxylamine, NH,OH, might be present in some sea waters was investigated by Fiadeiro et al. (1967), who found that at oxygen concentrations greater than 0.05 ml/l, it was too unstable for any appreciable concentrations to accumulate.

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D.

S. CORNER A N D ANTHONY 0 . DAVIES

B. Physico-chemical reactions Most of the fixcd nitrogen in thc sca is iiivolvcd in a continuous cycle in which plankton organisms play an important part. The biological processes involved arc tlic subjects of later sections, but it is worth noting a t this point that interchange between the inorganic forms of nitrogen may also result from physico-chemical reactions. Thus, Vaccaro (1962) found that the oxidation of ammonia to nitrite in aerated sea water kcpt in the dark occurred within 48 hours. The rate of oxidation was higher in water enriched with ammonia or to which mixed plankton had been added, so that whereas a ten-fold increase in nitrite took about 2 days in an unenriched sample, it required only 0.52 days in one that was enriched. Although the possibility that this oxidation had been caused by bacteria could not be excluded, the numbers of microorganisms present were thought t o be too small to explain the relatively fast reaction. The photo-oxidation of ammonia in sea water has also been described (e.g. Rakestraw and Hollaender, 1936), but Hamilton (1964) was unable t o confirm this finding. The absence of a catalytic surface from the water used in Hamilton’s experiments may have caused the difference, but he concluded that, even with catalysis, photo-oxidation was unlikely t o play an important role in the marine nitrogen cycle. On the other hand, he found that photo-reduction of nitrate t o nitrite took place in sea water, 0.60 pg-atoms NO;-N/l appearing in a sample containing 15 pg-atoms NO;-N/1 after one day’s exposure t o sunlight. C. Organic nitrogen Organicslly-bound nitrogen, present in particulate form (e.g. phytoplankton or zooplankton) is eventually released into the sea by processes such as excretion by zooplankton, and the decomposition of marine organisms in general. The most important group of dissolved nitrogen-containing organic compounds are the amino-acids and Degens et al. (1964) identified 17 of these in the Pacific Ocean off California. Concentrations of the individual acids in the surface waters ranged between 0.7 and 12-Opg/land increased slightly with depth. The spectrum of acids varied little throughout the water column, the predominant members being serine (29.5y0), glycine ( 16-4y0), ornithine (14.5%) and a-alanine (10.7%). Chau and Riley (1966) found somewhat higher concentrations in the Irish Sea (individual values lying in the range 2 to 16 pg/l), and some differences in the acid spectrum were also apparent. Thus, Chau and Riley did not detect ornithine or histidine in their samples, but did find mcthionine which was not reported by Degens el al (1964).

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D. Inorganic phosphorus Currently used analytical methods allow the measurement of three main types of phosphorus in the sea (Strickland and Austin, 1960). They are (1) dissolved inorganic phosphate; (2) dissolvcd organic phosphorus; and (3)particulate phosphorus, both inorganic and organic. However, because of the non-specific nature of the analytical techniques, these divisions are by no mcans clear-cut (e.g. inorganic phosphate polymers arc included in dissolved organic phosphorus). The dissolved inorganic phosphate is represented almost cxclusively by orthophosphate. The apparent dissociatioI1 constants of phosphoric acid determined by Kcster and Pytkowicz (1967) indicate that in sea water of salinity 33x0 a t 20°C, most of the orthophosphate (87%) would be present as HPOt- with 12% as PO:- and the rcmainder as H,PO;. Sillen (1961), using data on the solubility of the various forms of calcium phosphate, speculated that the orthophosphate in deep sca water, away from any biological influence, might be in equilibrium with the mineral, hydroxyapatite, which is present in marine sediments: Ca,(PO,),OH(s)

+ 4H+ + 5Ca2+ + 3HPOt- + H,O.

By using ultra-violet irradiation t o oxidize the dissolved organic phosphorus to orthophosphate, Solbrzano and Strickland ( 1968) were able t o show that polyphosphates, which were resistant to the irradiation, were only rarely present at levels above the detection limit of 0.05 pg-atoms P/1 in sea waters obtained off the California coast and also from the east-central Pacific Ocean. A similar finding has been reported for English Channel water by Armstrong and Tibbitts (1968).

E. Organic phosphorus Although the organic fraction may represent more than 50% of the total phosphorus in solution, its chemical constitution has yet t o be described. Strickland and Austin (1960) found that dissolved organic phosphorus concentrations were highest when phytoplankton populations were large, indicating that its release by plankton or formation during their decomposition was probably its main source. Strickland and Sol6rzano (1966) found little of the organic phosphorus to be present as enzyme-hydrolysable phosphate esters and suggested that it might be nucleic acid material. The fact that substantial quantities of deoxyribonucleic acid are present in particulate matter in the sea (Holm-Hansen et al., 1968) lends support t o this view.

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

111. THE STOICHIOMETRY OF BIOLOGICALLY INDUCED CHANGESIN NUTRIENT LEVELS “ It is a remarkable fact that plant growth should be able to strip sea water of both nitrate and phosphate, and that in the English Channel the store of these nutrient salts formed during the autumn and winter should be used up at about the same time ”, wrote H. W. Harvey in 1926. The implication, that the concentrations of the two nutrient salts in the sea were apparently in the ratio in which they were assimilated by the phytoplankton, was taken up some years later by Redfield (1934). He showed that there was, in fact, an approximately linear correlation between the concentrations of nitrogen (as nitrate) and phosphorus (as phosphate) for sea waters obtained from many different geographical locations and different depths. The lowest concentrations werc found in the surface layers, where the nutrients had been utilized by the plants; and their near proportionality meant that complete assimilation by the phytoplankton of one of the nutrients would leave very little of the other unused, in agreement with Harvey’s observation. The metabolism of organic matter by animals and bacteria releases into solution organic forms of nitrogen and phosphorus as excretion products which are eventually oxidized back to nitrate and phosphate ions, oxygen being consumed in the process. During photosynthesis, on the other hand, the nutrient salts are utilized for the synthesis of organic matter by plants, and oxygen is produced. Redfield (1934) argued that the relative changes in the concentrations of inorganic nitrogen and phosphorus in sea water resulting from these biological changes should be directly related t o the elementary composition of the plankton. He showed that, while there was a considerable variation between species, the average nitrogen : phosphorus ratio (by atoms) in a mixed group of phytoplankton and zooplankton was 18*7:1,this average being in good agreemcnt with the slope of 20:l given by the plots of dissolved nitrate-nitrogen against dissolved phosphatephosphorus.

A. The “ assimilation ratio ”, AN :AP Cooper (1937a) presented data which confirmed that the nitrogen: phosphorus ratios for sea water and marine plankton lay within close limits; but pointed out (Cooper 193th) that the technique used for phosphate analyses up to that time was subject to a salt error. When corrections were made for this, Redfield’s nitrogen :phosphorus ratio for sea water was reduced t o about 15:l. Cooper (1938b) further

PLANKTON IN NITROOEN AND PHOSPHORUS CYCLES

107

suggested that any deviations from this valuc should bc tcrmcd the I ‘ anomaly of the nitratc : phosphatc ratio ”. More recsnt work has indicated that, especially in coastal rsgions, the nitrogen : phosphorus ratio is frequently anomalous in this sense, and values of 5-1O:l are not uncommon, even during the autumn/ winter period when nutrient concentrations are maximal (e.6. Riley and Conover, 1956; Ketchum et al., 1958; McAllister et al., 19GO). Pratt (1965) found that, in Narragansett Bay, the ratio rarely exceeded 4:l and was more usually less than 1:l. Nevertheless, it is still generally true that nitrogen and phosphorus concentrations are linearly correlated with regression coefficients of between 15:l and 16:l so that, upon depletion of the nitrogen, some phosphorus remains. The slopes of these regression lines, AN: AP, represent the relative changes in the nutrient concentrations resulting from biological activity, and would be expected to reflect more closely the ratios of the nutrients taken up by the phytoplankton. The value of AN: AP has, therefore, been termed the I ‘ assimilation ratio ”. This ratio, AN: dP, can vary considerably from the usual valuc of 15 or 16:l. For example, Steftinsson (1968) has recently shown that although a value of 16.6:l was obtained when data for the Irminger Sea were treated collectively, therc was some variation with salinity, and the nitrogen : phosphorus relationship was better described by the expression [NO;-N] = 14-3 [PO:--P] 0.845 (S%, - 35) - 0.5. The AN: A P value of 14.3:l was rather lower than that usually found. Evidence exists that phosphorus utilization by phytoplankton continues after the nitrate-nitrogen concentration has fallen below the detectable limit. McAllister et al. (1960) followed the growth of a large scale culture of a natural population of phytoplankton and found that, as expected from the anomalous initial nitrogen :phosphorus ratio of 9-2:1,the nitrate was depleted before the phosphate. Growth continued, however, until the phosphorus had also disappeared, and assimilation ratios varied between 14:l when nitrogen was plentiful to 8 4 : l during the period of nitrogen deficiency. Indirect evidence that this also occurs in the sea is provided by the nitrate-phosphate plot of Ketchum et al. (1958) where the data for July and September (when the concentrations of nitrate were very low) indicate that nutrient assimilation was occurring at ratios much lower than the 15:l value which applied to the rest of the results. A similar finding has been reportcd by Steftinsson and Richards (1963) for the north-eastern Pacific Ocean. AN: AP values of 16:l were obtained at deep water (>1 000 m ) stations; but in the euphotic zone, values approaching zero resulted from phosphate assimilation after the exhaustion of the nitrate. The authors

+

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

suggested that regeneration of nitrogen might be the explanation of the continued growth, the rcmineralized form being used up very quickly so that inorganic nitrogen concentrations did not become detectable. Ketchuni et nl. (1958) thought that this remineralization occurred at depth, the nitrogen then being returned t o the euphotic zone by eddy diffusion. The possibility that the presence of ammonium-nitrogen might account for thc continued plant production was examined by Vaccaro (1963) for the waters off the New England coast. I n August 1962, although only trace levels of nitrite and nitrate-nitrogen were present in the euphotic zone, nitrogen : phosphorus ratios between 1:1 and 7 :1 resulted when ammonium-nitrogen concentrations were also taken into account. However, the AN: AP value calculated from the total inorganic nitrogen concentrat,ion was still low at 10.8: 1. Earlier in the year, the winter AN: AP value was surprisingly high at 20.8:l and only during the spring outburst in April was the value normal at 15.3:l.

Vaccaro (1963) showed that the atomic ratios N:P in the particulate matter suspended in the euphotic zone were similar t o the assimilation ratios: Particulate N/P AN/ AP value atomic ratios for water column (0-10 m) 11.2 Gulf of Maine, August 10132 10.8 South of Nova Scotia, April 1962 16.6 15.3 Higher nitrogen : phosphorus ratios were obtained for the particulate matter gathered from deeper waters: these were thought t o be due t o a more rapid loss of phosphorus than of nitrogen during the remineralization of the organic detritus. The small seasonal variation of the particulate nitrogen : phosphorus ratio discovered by Vaccaro is similar t o that found previously by Harris and Riley ( 1956) for phytoplankton collected over the period of a year from Long Island Sound. Here, the nitrogen : phosphorus ratios only varied between 20: 1 in February t o a little over 13:1 in midsummer (See Table I). During the same period the nitrogen : phosphorus ratio (excluding ammonium-nitrogen) in the sea water had decreased from about 8: 1 a t the winter maximum t o approximately zero after the spring bloom (Riley and Conover, 1956). Harris and Riley’s average ratio of 16*2:1was in good agreement with the value of 16:l originally proposed by Fleming (1940) and which is now usually regarded as representing the average nitrogen : phosphorus ratio in marine plankton (Redfield et al., 1963). Direct experimental support for this ratio has been pro-

PLANKTON I N NITROGEN A N D PIIOSPIIORUS CYCLES

109

vided by Grill and Richards (1964) who followed the rate of nutrient regeneration from decomposing phytoplankton which had been cultured from an inoculum of mixed plant cells obtained from the sea. For much of the decomposition period, nitrogen (as ammonia) and phosphorus (as phosphate) were released in the ratio of 16:l. TABLEI. SEASONAL VARIATION IN NITROGEN AND PHOSPHORUS CONTENTS AND IN THE N : P RATIOOF PHYTOPLANKTON FROM LONGISLAND SOUND I N 1963. (Data from Harris and Riley, 1956)

yo Dry

Weight

Date Nitrogen Phosphorus

N:P (Atoms)

-

Main species present (aapercenfqe of total cell count)

_-____

__.

Jan. 27 Feb. 18 Mar. 9 Mar. 23 June 1 July 7(a) July 7(b) Aug. 4 Fob. 1

2.25 2.33 2.87 2.09 4.77 4.15 4.43 2.73 2.24

0.33 0.26 0.36 0-27 0.73 0-57 0.64 0.48 0.32

15-1 :1 19.8:l 17.6:l 17.1 :1 14.4:l 16*2:1 1!5.5:1 12*6:1 15.5:l

Average

3.10

0.44

16*2:1

Code

A B C D E

A, 72.1 ; B, 8.1 ; D, 9.6 A, 82.7 ; D, 8.2 A, 96.0 A, 72.2 ; C, 8.7 ; E,8.9 G, 6.0; L, 18.0: P, 53.3 F, 26.0; H, 8.7; Q, 43.8; It, 6.1 F, 14-3; M, 34.5; Q, 32.1 ; R, 10.8 J, 8.6 ;K, 5.9 ; L, 64.0 ;N, 8.7

-

Skeletonenaa costatum (Grcvillc) Clovo T h a h s w e i r a decipiens (Van Hciirck) Jorgonsoii T . nordenakioldii Clcvo Thalassionema nitzschioides Hustcdt Lauderia borealis Gran P Nitzclchia closterium (Ehrcnbcrg) Wm. Smith G N . pungena var. dlantica Clcvo H Asterionella j a p o n k Gran J Chaetoceros afine Lauder K C . curvisetum Clcve L C . decipiena Clcvc M Coscinodiscw centralis var. paci&u Gran & Angst N Prormntrum scutellum B. Schroder P Peridinium trochoideum (Stcin) Lcmm. Q Gonyaulax africana Schiller R G . cochlea Mew.

B. Apparent oxygen utilization The concept of " apparent oxygen utilization " (AOU), first introduced by Redfield (1942), is increasingly being used in connection with the stoichiometry of nutrient changes brought about biologically. It is

110

E. D. S. CORNER AND ANTHONY

a. DAVJES

based upon the idea that a mass of water at the sea surface should be in equilibrium with the atmospheric oxygen, the solubility of which is a function of temperature and salinity. When this mass of water sinks below waters of lower density, the oxygen content is presumed t o remain constant in the absence of biological activity. Any difference between the measured oxygen content of the water and that expected for water of the same salinity and temperature is called the “ apparent oxygen utilization ” and represents the oxygen used for the remineralization of organic matter (AOU positive), or the oxygen produced during photosynthesis (AOU negative) or, possibly, the sum of the two. The AOU should thus be stoichiometrically related to changes in the nitrogen and phosphorus concentrations in the same water mass which, in turn, should reflect the atomic ratios in the plankton. The ratios now generally in use are dO:[dC:dN:AP] = - 276:[106:16:1] Those within the brackets were suggestcd by Fleming (1940) as average values for marine plankton, and the oxygen ratio is based on the assumption that, for the mineralization of the organic matter, the ratios dO/dC = 2 and dO/dN = 4 apply (Redfield et al., 1963). Phosphorus is considered to be completely in the form of phosphatc and so requires 110 oxygen for regeneration. If the carbon is assumed to be present &s carbohydrate and the nitrogen in the amino form, the above ratios correspond to the overall reaction (Richards, 1965): ( C H 2 0 ) 1 0 6 (NH3)16

H3P04

+106C0, + 122H20 + 16HN03 + H,P04. 13802

=

There are two main factors which can give rise to deviations from the expected oxidative ratio. The first, of much importance in the euphotic zone, is that oxygen produced by photosynthesis may result in supersaturation of the surface layers so that some oxygen could be lost to the atmosphere. The second is that the water mass under consideration is likely to have contained some nutrients before sinking: so that the total measured nutrient then consists of that originally present (the “ preformed nutrient ”) and that of oxidative origin (the ‘‘ regenerated nutrient ”). Both of these effects may lead to oxidative ratios which are lower than those predicted. Stefhnsson and Richards (1964)examined the relationship between the ‘‘ apparent phosphate uptake ” (APU) and the “ apparent oxygen production ” (AOP). The APU was the difference between the observed phosphate conrentration and that occurring in water, at the same station, which w a s just saturatcd with oxygen (i.c. in which the phos-

PLANKTON I N NITROGEN AND PHOSPHORUS CYCLES

111

phate and oxygen appeared to have behaved conservatively) : the AOP was simply the negative value of the apparent oxygen utilization. It was found that during the spring, most of the APU values agreed, within f 0.1 pg-atoms/l, with the value expected from the AOP :APU ratio of -276 :l. The APU values for offshore water in early summer were considerably lower than would have been expected, on the basis of the same ratio, from the AOP values; and Stefhnsson and Richards suggested that loss of the oxygen to the atmosphere accounted for this. There was, however, at the same time, a reasonable correlation between the APU and the AOP for inshore waters: indicating that photosynthesis was the predominating factor regulating the nutrient concentration in this region. The measured nutrient levels in the sea represent the sum of the preformed and the regenerated concentrations so that, using the oxidative ratios given earlier, one may write for phosphate (P) and nitrate (N) : P,,,, = Pprer Po, = Ppref 0.0036 AOU and N,,,, = N,,,, No, = N,,,, 0.058 AOU. Thus, a plot of measured nutrient concentrations against AOU values should be linear, and the intercept at zero AOU would correspond to the preformed nutrient concentration (at the depth appropriate to AOU = 0). It has been pointed out (Pytkowicz, 1968) that, hidden in these equations, is the assumption that the oxygen concentration in a mass of water is equivalent to the sum of the fractional contributions to the total oxygen content by each water type which mixed to form the mass, and that this assumption is true only if the water types are similar in temperature and salinity. I n practice, however, the error introduced, even if the water types have different characteristics, is usually small and Park (1967) showed that the nutrient and oxygen concentrations present in the sea off the Oregon coast were in good accord with these equations. Broenkow (1956) reported measurements of AOU values and nutrient concentrations in the Costa Rica dome, a region of upwelling in the eastern tropical Pacific Ocean where deep waters with higher than normal salinities and nutrient levels but lower oxygen concentrations are brought to the surface. The AN :LIP value of 16.5 :1 was normal and independent of depth, but the AAOU :AP ratio gave two values, namely -274 :1 for water obtained above 120 m and -114 :1 for water below this depth. Broenkow was able to show that loss of oxygen to the atmosphere was significant only in the upper 20 m and the points even for these depths were within the confidence limits of the calculated regression line, The lower ratio found for the deeper waters

+

+

+

+

112

E. 1). 8. CORNER AND ANTHONY G I . DAVIES

was explained by the presence of preformed nutrients, the concentrations of which increased with depth. Broenkow suggested that the results for the deeper waters might be explained by the mixing of two water masses, one with a low and the other with a high nutrient concentration. There would then have been no reason for the AAOU :AP relationship t o be linear. Sugiura (1965) suggested that, as the preformed phosphate concentration is a conservative property of sea water, it would be preferable, in constructing plots of phosphate concentration against AOU values, t o use data for water masses having similar conservative properties, e.g. temperature and salinity. When this was done, AAOU :AP values of -272 :1 were consistently obtained for the waters of the Oyashio and Kuroshio regions (Sugiura and Yoshimura, 1964). Although the values for apparent oxygen utilization in many different regions seem consistent with Fleming’s ( 1940) original ratios, more recent data has cast doubt on the extent t o which his C :N :P ratios of 106 :16 :L are truly representative of plankton. Thus, out of eleven species of phytoplankton grown in culture and analysed by Parsons el al. (1961), only two-Cricosphuera carterae (Braarud c t Fagerl.) Braarud [as Syracosphuera carterae] and Coscinodiscus sp.-contained nitrogen and phosphorus in ratios near 16:1, the majority of values being much lower (see Table 11). The common diatom Skeletonema costatum (Greville) Cleve, for example, had a ratio of 7.7 :1. Although it TABLE11. THE NITROGEN AND PHOSPHORUS CONTENT AND THE NITROOENPHOSPHORUS RATIOIN SOME CULTUREDSPECIESOF MARINEPHYTOPLANKTON. (Data from Parsons el al., 1901.)

yo Dry weight

h

Tetraaelmia maculata Butch. Dunaliella salinu (Dunal) Teodor. Monochrysia lutheri Droop Syracosphaeru curterae Braarud et Fagerl. Chaetoceros sp. Skeletonema costalum (Grovillo) Cleve Coscinodiactu, sp. Phaeodactylum tricornutum Bohliti Amphidinium carterue Hulb. Exuvietla sp. A gmen ell um q umlr uplicat um (Meiiogh ) I3r6b .

.

8.3 9.1 7.8 8.9 5.6

5-9 2.7 5.3 4.5 5.0 5.8

3.3 3-3 3.0 1.2 1.6 1.7 0.4 2.0 1.1 1.3 1.4

5.5 :1

6.1 :1 5*8:1 17.4 :1 8*3:1 7.7:1 16*0:1

5-9:1 13-2:l 12.3:l 10.6:l

PLANKTON IN NITROGEN AND PHOSPHORUS CYCLES

113

could be argued that these low values may have reflected the fact that the plants had been cultured in the laboratory, certain data obtained for natural populations of phytoplankton have also been inconsistent with Fleming's ratios. Thus, coastal phytoplankton studied by Antia et al. (1963) were found t o have C :N :P ratios varying from 85 :16.5 :1 to 52 :13.5 :1 , the former when nitrate was depleted and the latter when nitrate was present in excess. Furthermore, an oceanic population analysed by McAllister et al. (1960) gave ratios of 86 :17 :1 when nitrate was plentiful: for this the oxidative ratio d0:dP would be only -240:l.

Later in this review (Section I X ) it will be seen that the atomic ratio nitrogen : phosphorus in zooplankton can also vary considerably ; but the data obtained by Beers (1966) for mixed zooplankton collected from the Sargasso Sea are worth quoting in the present context. Copepods and chaetognaths, which together comprised the greater proportion of the total population, had nitrogen : phosphorus ratios greater than 27 :1 and, on the basis of these data, Holm-Hanscn et al. (1966) suggested that realistic average C :N :P ratios for zooplankton (allowing for a preponderance of copepods) would be 117 :23 : l . Why many values for apparent oxygen utilization (AOU) are consistent with Fleming's (1 940) atomic ratios, but certain data for C :N :P in plankton are not, is a question that deserves further study.

IV. UPTAKE OF NITROGEN COMPOUNDS BY PHYTOPLANKTON For much of the year in temperate regions, and almost permanently in tropical sca areas, the water above the thermocline contains low levels of dissolved nitrogen and phosphorus compounds. In this situation, plant production is dependent upon the nutrients supplied by regeneration and vertical transport, and the growth of those species which can most efficiently assimilate and utilize the low concentrations which become available should be favoured. For this reason, them is currently a great interest in understanding the relationship between phytoplankton growth and nutrient levels, as this is likely to be an important factor in determining species succession and geographical and temporal variations in natural populations.

A. Inorganic forms of nitrogen In general, organic forms of nitrogen such as amino acids do not appear t o be satisfactory nitrogen sources for phytoplankton growth (Harvey, 1940; Guillard, 1963); and although urea and uric acid are utilized by some coastal and estuarine species, these compounds are

10

12

14

ooys

FIG.1. The variation in ammonium and nitrate ion concontrationsand tho production of chlorophyll a and nitrate reductase (NR)during the growth of Cnchoaina niei in the deep-tank cultures studied by Strickland el al. (1969) and Epploy el al. (1969a). See text for full description. The unit of nitrate reductase activity wm that which formed lo-* moles NO;/pg chlorophyll a/hour. (After Eppley el ul. 1969a.)

115

PLANKTON IN NITROGEN AND PHOSPHORUS CYCLES

not likely t o be of much significance in the marine nitrogen cycle because of their very low levels in the sea. Accordingly, our attention will be directed towards the inorganic forms of nitrogen only. When nitrate is utilized as a nutrient, it is reduced stepwise within the plant cells through nitrite, hyponitrite, hydroxylamine and ammonia before the nitrogen is finally incorporated into the cellular material (Nicholas, 1959). This reduction is an energy-consuming process, the OH2 0 2 inoverall reaction NO, + H + + 2H20---tNHf volving a free energy increase of 77.4 k cals/mole a t 25OC (Cooper, 19373). It is not surprising, therefore, t o find that when both ammonia and nitrate are present in culture media, ammonia is used preferentially by phytoplankton. The most recent demonstrations of this are those of Grant et al. (1967) using the diatom Cylindrothecu closterium var. Culifornica (Mereschk.) Reimann e t Lewin, and of Strickland et al. (1969) who worked with large-scale, deep-tank cultures of Ditylum brightwellii (T. West) van Herck, Cachoninu niei A. R. Loeblich, 111, and a mixture of Gonyaulux polyedra Stein and Phaeocystis sp. The variation in the concentrations of the two forms of nitrogen observed by Strickland et al. during the growth of the dinoflagellate Cachonina niei is illustrated in Fig. 1. The increase in chlorophyll a resulting from plant growth was accompanied in the early stages by a decrease in the ammonia concentration only; but on the sixth day, when the ainnionium-nitrogen had been reduced t o about 1 pg-atom/l., nitrate and ammonia were both utilized. Similar events occurred in the other deep-tank cultures. Eppley et al. (1969e) using the same cultures as Strickland et al. found that nitrate assimilation was associated with the production, within the cells, of the enzyme nitrate reductase (Fig. 1). This enzyme was initially absent, as the stock cultures were grown on nitrite. On the eighth day of the Cachoninu culture, the cells were allowed t o migrate t o the surface by stopping the mixing and it was possible t o replace most of the original culture medium by sea water of low nitrate content without losing the phytoplankton. This resulted in the almost complete disappearance of the nitrate reductase from the cells until addition of nitrate t o the culture on the 13th day caused a dramatic rise in the enzyme activity. Eppley et al. have suggested that the discrimination between nitrate and amnionia as nitrogen sources was because the formation of nitrate reductase was repressed a t the levels of ammonia initially present in the culture medium. I n the sea, on the other hand, ammonia concentrations are normally so low that this repression should not occur, and Eppley et al. were able t o detect nitrate reductase activity in sea water

+

A.Y.B.--B

+

6

iis

'E. D. 9. CORNER AND ANTHONY CI. DAVIES

collected from the tropical Pacific Ocean (though they could not positively associate the enzyme exclusively with the phytoplankton). Further, the simultaneous uptake of ammonia and nitrate which would be expected under natural conditions has been observed by Dugdale and Goering (1967)who used [16N]-labellingto follow the assimilation of these nutrients by phytoplankton populations obtained from several sea areas. In all cases, both iiutrients were taken up simultaneously though the average of the specific ratcsof dark and lightnitrate uptake, NO; (expressed in terms of particulate nitrogen concentration instead of cell population), was always lower than the average of the specific rates of ammonia uptake, B N H ~In. Table 111, values of ~ N O Jare TABLE111. THEAVERAGE NITRATZ UPTAKE EXPRESSED AS A PERCENTAQEOF THE TOTAL NITROGEN UPTAKEBY NATURAL PHYTOPLANKTON COMMUNITIES IN V~RIOUS SEAAREAS. (Data from Dugdale and Goering, 1967.)

Area .

NE Pacific Coast, Seattle- Juneau NE Pacific Coast, Juneau-Cape Spencer N Pacific, Vancouver-Honolulu NW Atlantic, Georges Bank-Caribbean Sargasso Sea, Station S NW Atlantic, Gulf of Maine

Sep. 1964

20.3

Nov. 1964

27.6

Feb. 1965

8.7

Mar. 1962 Sep. 19G2-Jan. 1963 Apr. 1963

28.8 8.3 39.5

expressed as a percentage of the total uptake due to both forms of nitrogen, i.e. 100 ~ N N O ; ( ~ N O ; ~ N H : ) . Considerable monthly changes in this fraction were observed at Station S in the Sargasso Sea near Bermuda, the average specific rate of nitrate uptake varying from a minimum of 0.5% of total uptake in early November to 18.9% in late January. Dugdale and Goering showed that the relative increases in nitrate assimilation occurred at times of comparatively high nitrate concentrations in the euphotic zone.

+

B. The effect of light Nutrient assimilation by the natural phytoplankton populations examined by Dugdale and Goering (1967) took place in the dark as well &B

P W K T O N IN NITROGEN AND PHOSPHORUS CYCLES

117

the light, though at a lower rate. Thus, for tropical phytoplankton the specific rate of ammonia uptake in the dark was only 0.6 of the light value, and for nitrate the fraction was only 0.3. There is in fact evidence that light is involved in nitrate reduction within plant cells. Thus, Eppley and Coatsworth (1968) found that cultures of Ditylum brightwellii containing little nitrate reductase took up nitrate in both the dark and the light. However, in the dark, the rate of uptake decreased over a period of two hours and most (84%) of the nitrate accumulated could be recovered from the cells unchanged. In the light, on the other hand, the rate of uptake remained constant over the same period and only 44% could be recovered. Further, as no nitrite could be detected in the cells, Eppley and Coatsworth concluded that the reduction had proceeded beyond this stage and pointed out t h a t the rate of reduction (0.5 pg-mole/lOs cells/h) was higher than could be accounted for by the low level of nitrate reductase activity within the cells. It therefore appeared that a light-induced reduction was occurring. This view was supported by the previous work of Grant (1967) who showed that the rate of nitrate assimilation by Dunuliella tertiolecta Butch. is a function of light energy. The effect of light upon nitrite uptake is less clear, for whereas Ditylum brightwellii did not assimilate this form of nitrogen in the dark (Eppley and Coatsworth, 1968), Dunuliella tertiolecta did (Grant, 1967), and Vaccaro and Ryther (1960) found that at low light energies, phytoplankton may even secrete nitrite. C . The hyperbolic relationship Probably tho first investigation of the rate of nutrient uptake by a marine phytoplankton species was made by Ketchum (1939a). Using cultures of the diatom "Nitzschia closterium forma minutissimu " (now P k m t y l u m tricornutum Bohlin) it was shown that the rate of nitrate uptake in the light, measured over a short period, varied hyperbolically with the nitrate concentration in the medium, increasing rapidly with rising concentration at low nitrate levels, then less quickly at higher levels and finally reaching a maximum value above about 14 pg-atoms NOi-N/l. Until recently, evidence that this hyperbolic relationship between the rate of uptake of a nutrient and its concentration holds generally waa still limited ;but for nitrogen compounds it has now been shown to apply to nitrite and nitrate assimilation by Ditylum brightwellii (Eppley and Coatsworth, 1968), and for the uptake of nitrate and ammonia by a wide range of species in culture (Table IV) (Eppley et al.,196913). In addition, MacIsaac and Dugdale (1969) were able to demonstrate,

118

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

using [15N]-labellednutrients, that a hyperbolic relationship also applies in the case of uptake of nitrate and ammonia by natural phytoplankton communities (see Table IV). Curves like those in Figs. 2 and 3, examples from the work of Eppley et al. (1969b),are described by an equation relating the rate of removal of

5, NO3 concentration

(VM)

FIG.2. The rate of nitrate uptake ( a ) by Coscimdiscm Eineaitcs as a function of the nitrate concentration(8) in the medium. The intercept of the S / u line on the abscissa corresponds to the negative value of the half-saturation constant for uptake K i . (After Eppley et d., 1969b.)

the nutrient from the medium ( v ) to its concentration (S)and having the form v = - dS - V,NS dt K:f f S' The variables are S ; N, the cell population ; and t , the time. The constants are V,, the maximal specific uptake rate (equal to v/N when S K:) and K,", now usually called " the half-saturation contant ". K: is the value o f S corresponding to an uptake rate of one half the maximal value, and provides a quantitative measure of the ability of a phytoplankton species t o assimilate nutrients, especially at low concentrations.

>

PLANKTON IN NITROGEN AND PHOSPHORUS CYCLES

119

S. N H t concentration (wM)

FIO.3. The rate of ammonium uptake (v) by Rhirosolenin robilala as a function of the ammonium concentration (S) in the medium, and the linear t.ranaformationof the data which provides the haltsaturation constant. (After Eppley el. al., 1969b.)

The form of this equation is the same as that occurring in the Langmuir adsorption isotherm and in Michaelis-Menten enzyme kinetics; but as the mechanism of uptake is unknown there is no justification at the present time for assuming that the uptake equation results directly from surface or enzyme promoted nutrient transport, though both will undoubtedly be involved. Values of the two constants may be obtained using a linear transformation of the equation, for which several forms are possible, that used by Eppley et al. being

8 = NV,,,(S/v)- K,". Thus, for a constant population N, plots of Slv against S should be linear, the intercept on the abscissa corresponding to -K:. The results of such a transformation are also illustrated in Figs. 2 and 3, and the values of

K: obtained by Eppley et al. in this way are reproduced in Table IV, together with those obtained for natural populations by MacIsaac and Dugdale (1969). Eppley et al. (196913) have pointed out several interesting features in the data : (1) that a high K,"value for nitrate uptake is usually associated with a high value for ammonia uptake; (2) that larger species, which tend to grow more slowly, in general have higher

TABLEIV. HALF-SATWATION CONSTANTS FOB (K:) OF NITRATEAND AMMONIUMIONSBY ~ I N PHYTOPLANKTON E SPECIES IN C a m r AT 18°C (Data from Eppley e t d . , 1969b) AND BY NATUE~AL POPULATIONS (Data from MacIassc and Dugdale, 1969). Units of K,"are pmolesll. Where only one value is given, data from two experiments were combined. Nitrate Organim Oceanic species Coccolithwr huxleyi" C . huxleyib Chaetoceroa gracile Cyclotella nana Neritic diatoms Skeletonema coelatum Leptocylindrua danicw Cleve Rhizocrolenia atolterfothii H.Peragallo R. robwrta Pritchard Ditylum brightwellii Coacinodiscw lineatw Ehrenberg C . wailesii Gran & Angst Aaterionello j a p o n k Neritic or littoral flagellates Qonyauhx polyedra Gymnodinium aplendena Lebour Monochyaia lutheri Isochryaia gdbana Dunaliella tertwlecda Natural marine communities Oligotrophic Eutrophic a

Sargaaso Sea isolate

D

Oslo Fjord ioolate

K:

Ammonium

Ii:

f95y'O conf. limit

i95% conf. limit

0.1 0.1 0.3, 0.1 0.3, 0.7

0.3 1.6 0.5, 0.2 0.4, 0.5

0.1 0.2 0.5, 0-3 0-4

0.7 0.9 0-5, 0-3 0.3

0.5, 1.3, 1-7 3.5, 0.6 2.4, 2.1, 0.7,

0.4, 0-1 0.5, 0.1 0.4 1.0, 1-0 1.7 0.5, 0-6 0-3, 1.8 0.3, 0.5

3.6, 3.4, 0.5, 5.6, 1.1 2.8, 4.3, 1.5,

0.8, 0.7, 0-5 1.4, 0.2, 0-4 0.9, 0.4 2.0, 1.5 0.6 2.6. 1.0 5.4, 2.0 1.2, 0.8

- 2.4 0.9 0.3 0.2, 0.2 1-1

5.7, 5.3 1.1 0.5

0.6, 1.1 1.0 0.4

0-1

0-6

0.4 1-2 2.5 2.8 5-1 1.3

8.6, 10.3 3-8 0.6 0.1, 0.1 1.4 0.2 (G expts) 1.0 (3 expts)

0.8. 0.8 0.9, 0.5 0.5 9.3

1.2 5.5 0.6

-

0.1-0-6 (3 expts) 1.3 (1 expt)

I

Cell diameter (P)

5 5 5 5

8 21

20 85

30 50 210

10 45 47 5 5 8

PLANKTON I N NITROQEN AND PHOSPHORUS CYCLES

121

K t values; and (3) that oceanic species usually have low K: values, which would be in accord with their need to assimilate nutrients at the low concentrations present away from the land. This is also in agreement with the low values obtained for the natural populations observed by MacIsaac and Dugdale (1969). Surprisingly, euryhaline species such as Dunaliella tertiolecta and Momchrysis lutheri usually had low K: values also, even though their natural habitat would normally be expected to have high levels of nutrients.

V. UPTAKEOF PHOSPHORUS COMPOUNDS BY PHYTOPLANKTON A. Inorganic forms of phosphorus Probably because phosphate is less often a limiting nutrient, its uptake by marine phytoplankton has not been studied in as much detail as that of nitrate. Phytoplankton in culture media where the phosphate concentration is limiting continue to grow long after the nutrient has been stripped from solution, albeit at a gradually reducing rate (Ketchum, 1939b; Goldberg et al., 1951 ; Kuenzler and Ketchum, 1962). It thus appears that cells are able to accumulate phosphate in excess of their immediate requirements, and to utilize this store at times of nutrient depletion in the external medium. Ketchum (1939b) showed that Phueodmtylum tricornutum can replenish this reserve by taking up phosphate even in the dark. The amount of the nutrient absorbed by the cells in this way (between 1.1 and 8-6 x lo-* pg-atoms PO:--P/cell) increased with the length of time for which the cells had utilized their phosphate reserve, and a constant cellular concentration independent of the phosphate level in the medium was finally attained. The uptake of phosphate by depleted cells is a very rapid process. Kuenzler and Ketchum (1962), for instance, found that in 12 hours an increase from 4 to 66 x pg-atoms PO:--P/cell could take place in illuminated cultures of Phaeodaetylum tricornutum from media with During the initial concentrations of 30 or 80 pg-atoms PO:--P/I. ensuing growth of the cultures, phosphate was completely removed from the media and there was a gradual diminution in the cellular concentration. Goldberg et al. (1951) showed that the phosphate content of exponentially growing cells of Asterionella japonica was a linear function of the level in the culture medium. However, up to 50% of the phosphate absorbed appeared to be only loosely bound into the cells, as it was readily exchangeable.

B. Organic forms of phosphorus Organic phosphate esters may also provide a source of phosphorus for phytoplankton (Chu, 1946; Harvey, 1953). Kuenzler and Perras

122

E. D.

9. CORNER AND ANTHONY Q. DAVIES

( 1965) have demonstrated that under phosphate-deficient conditions, the enzyme alkaline phosphatase is produced within phytoplankton cdls ; but that when external phosphate concentrations are adequate for growth, formation of the enzyme is suppressed. This enzyme has the ability t o hydrolyse organic phosphate esters, and it was shown that its presence within cells enables them t o utilize the phosphate portion of such esters. The rate of uptake of phosphate from tlirce different types of ester (glucose-6-phosphate,adenosine monophosphate and a-glyceropliospliate) was found t o be the same for a given phytoplankton species, indicating that a similar uptake mechanism was operating for all three compounds. Apparently only the phosphate portion was absorbed by the cells, the organic portion remaining in the culture medium. This probably indicates that the site of action of the enzyme was on or near the exterior surface of the cells. Although the organic forms of phosphorus in the sea remain to be identified, some will almost certainly be present as phosphate esters. Kuenzler and Perras (1965) have suggested that the ability of phosphate-deficient phytoplankton t o utilize this source of the nutrient could be of considerable importance: for the rate at which phosphate can be recycled in the euphotic zone would be greatly increased if complete remineralisation were unnecessary. However, the levels of enzyme-hydrolysable organic phosphate found by Strickland and SolGrzano (1966) in coastal waters were very low (0.03-0.45 pg-atoms P/l), though this could have been due t o rapid utilization of these phosphate esters. The quantitative relationship between the rate of phosphate uptake by phytoplankton and the concentration of the nutrient in sea water has yet t o be established ; but the early work of Ketchum (19394 indicates that it is also hyperbolic in form. Interestingly, this work demonstrated that phosphate uptake rates are also hyperbolically related t o the nitrate concentration of the medium.

VI. THE EFFECTOF NUTRIENT LEVELSON PHYTOPLANKTON GROWTH KINETICS Although the comparative growth rates of various phytoplankton species under nutrient limiting conditions are likely to have a great bearing upon seasonal variations in the species composition of the phytoplankton, the quantitative relationship between the division rate of the phytoplankton population and the available nutrient concentration is not, at present, well defined. Insome cases,an equationhaving the same form as that described for uptake appears t o hold : Eppley and Thomas (1969), for instance, have shown that the growth rates of Asterionella

PLANKTON IN NITROGEN AND PHOSPHORUS CYCLES

123

juponica and Chuetoceros gracile Schiitt vary hyperbolically with the nitrate level in the culture medium. There is also evidence, however, that the nutrient content of the phytoplankton cells may be the factor which determines their division rate: this has been shown for the phosphate-limited growth of Phueoductylum tricornutum (Kuenzler and Ketchum, 1962), for the nitrate-limited growth of Isochrysis galbaiza Parke (Caperon, 1968), for the vitamin B,,-limited growth of Monochrysis Zutheri (Droop, 1968) and for the iron-limited growth of Dunuliella tertiolecta (Davies, 1970). I n the latter three cases, a hyperbolic relationship between the growth rate and the cellular content of the limiting nutrient was demonstrated. That nutrient uptake and cell growth are not directly related has long been recognized. Ketchum (1939a), for instance, found that a decrease in nitrate concentration which halved its rate of uptake by Phaeodactylurn tricornutum had no effect upon the rate of cell growth ; and recently it has been shown that the maximal rates of nitrate uptake by Asterionella japonica and Chuetoceros gracile arc mom than four times the maximal growth rates when the rates are expressed as doublings per day of respectively the cellular nitrate and the cell population (Eppley and Thomas, 1969). Eppley and Thomas have, however, demonstrated that if the specific rates of nutrient uptake, V, and of cell growth, p, are both assumed t o be hyperbolic functions of the nutrient concentration in the medium, i.e.

then the relationship between the specific growth rate and the cellular nutrient content depends upon the relative magnitudes of the halfsaturation constant for uptake K: and for growth K:. Using the steadystate relationship V = pQ where Q is the cellular nutrient content (Droop, 1968), they were able t o construct hypothetical curves which illustratc this (Fig. 4). These graphs show that only when the halfsaturation constants are equal is the specific growth rate independent of the cellular nutrient content, which would then remain constant despite variations in the nutrient level in the medium. I n the more usual situation of K: > 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).

126

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.

PLANKTON IN NITROGEN AND PHOSPHORUS CYCLES

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-

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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.

132

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

PLANKTON IN NITROGEN AND PHOSPHORUS CYCLES

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

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

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.

PLANKTON IN NITROGEN AND PHOSPHORUS CYCLES

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

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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

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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.

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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

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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

PLANKTON IN NITROGEN AND PHOSPHORUS CYCLES

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

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

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

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

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-

PLANKTON IN NITROGEN AND PHOSPHORUS CYCLES

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

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

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-

PLANKTON IN NITROQEN AND PHOSPHORUS CYCLES

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

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

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).

PLANKTON IN NITROGEN AND PHOSPHORUS CYCLES

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

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

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 -

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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.

PLANKTON IN NITROGEN AND PHOSPHORUS CYCLES

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-

PLANKTON IN NITROGEN AND PHOSPHORUS CYCLES

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

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

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.,

PLANKTON IN NITROGEN AND PHOSPHORUS CYCLES

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

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

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

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

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)

PLANKTON IN NITROQEN AND PHOSPHORUS CYCLES

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

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

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

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

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.

PLANKTON IN NITROGEN AND PHOSPHORUS CYCLES

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

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

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.

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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).

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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

PLANKTON IN NITROGEN AND PHOSPHORUS CYCLES

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

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

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)

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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.

PLANKTON IN NITROGEN AND PHOSPHORUS CYCLES

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.

+

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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

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

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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

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

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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FIQ.12. The seasonal variation of nutrients, chlorophyll u and zooplankton at a station in Harrington Sound, Bermuda. The nutrient data are the averages of observations at three depths (1, 7 and 14 m) and the chlorophyll u values correspond to a depth of 6 m: for zooplankton numbers, continuous line represents the total and the broken line copepode only. (After Beers and Herman, 1969; Herman and Boers, 1969.)

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.

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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

01

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Mor -Apr Dec- Jon Feb-Mor Aug-Oct Nov-Dec Dec-Jon Moy-Jul

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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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PLANKTON IN NITROGEN AND PHOSPHORUS CYCLES

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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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8W, Phosphorus N$ Nitrogen

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1962-63

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Dec

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C

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,

,

I .Mar

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FIG.15. The winter-spring variation in nutrients and plankton at a station (41'26.5" 71'25'W) a t the mouth of Narragansett Bay. I n each case, the data in A represents a vertical expansion of the values for the first four months shown in C. (After Pratt, 1965.)

25

0

PLANKTON IN NITROGEN AND PHOSPHORUS CYCLES

187

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

Phosphate phosphorus

40,

Chlorophyll

6 , Zooplankton volumes

5 4 E

\

3

2

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2

I

0 1952

1953

1954

FIG.16. Tho seaaonal variation of nutrients, chlorophyll and zooplankton in Long Island Sound. The data are the averages of weekly observations at four inshore stations. The solid line gives surface data, and the dotted line data for the bottom. The zooplankton volumes were obtained using an oblique tow (with 8 # 10 net) from near the bottom to the surface. (After Riley and Conover, 1956.)

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

E.

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

1'31

PLANKTON I N NITROGEN AND PHOSPHORUS CYCLES 0

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.

I

o

.

0

5

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2.5- 7.5 -0.050

-0.100

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o

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.

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.

175-200 M A M J J A S O, N D, J, F, a M A IM: JW J A S O N D J F M A

1952

1953

1954

FIO.17. The variation, with depth and mason, of the rate of change R (pg-atoms/litre/ day) of phosphate-phosphorus in Long Island Sound due to biological activity. Negative values of R indicate overall utilization and positive values overall regeneration of the nutrient. (Data from Riley, 1956b.)

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

s

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.

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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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Caporon, J. (1968). Population growth response of Isochrysie galbana to nitrate variation a t limiting concentrations. Ecology, 49, 866-872. Carpenter, E. J. (1970). Phosphorus requirements of two planktonic diatoms in steady statc culturc. J. Phycol. 6 , 28-30. Chau, Y. K. and Riley, J. P. (1966). The determination of amino-acids in sea water. Deep-sea Rea. 13, 111C1124. Chu, S. P. (1946). The utilization of organic phosphorus by phytoplankton. J. mar. biol. Ass. U . K . 26, 285-295. Conover, H . J . (1961). The turnover of phosphorus by Calanw finmarchicus. Addcndum to papcr by S. M. Marshall and A. P. Orr. On the biology of Calanwfinrnarchicw. XII. Tho phosphorus cyclc :cxcrction, egg production, autolysis. J. mar. biol. Ass. U . K . 41, 484-488. Conover, R. J. (1964). Food relations and nutrition of zooplankton. Occ. Publ. Narragansett mar. Lab. No. 2, 81-91. Conover, R. J. (1966a). Assimilation of organic matter by zooplankton. Limnol. Oceanogr. 11. 338-345. Conover, R. J. (1966b). Factors affecting the assimilation of organic matter by zooplankton and the question of superfluous fccding. Limnol. Oceanogr. 11, 346-354. Conover, R. J. (1968). Zooplankton-life in a nutritionally dilute environmcnt. A m . Zool. 8, 107-118. Conover, R. J. and Corner, E. D. S. (1968). Rcspiration and nitrogen excretion by some marine zooplankton in relation to thcir life cycles. J. mar. biol. ASS.U . K . 48. 49-75. Conover, S . A. M. (1956). Oceanography of Long Island Sound, 1952-1954. IV. Phytoplankton. Bull. Bingham oceanogr. Coll. 15, 62-1 12. Cooper, L. H. N. (1935). The rato of liberation of phosphate in sca water by the breakdown of plankton organisms. J. mar. biol. Ass. U.h'. 20, 197-202. Coopcr, L. H. N. (19378). On the ratio of nitrogen to phosphorus in the sca. J . mar. biol. Ass. U . K . 22, 177-182. Cooper, L. H. N. (1937b). The nitrogen cyclc in the sea. J. mar. biol. Ass. U . K . 22, 183-204. Cooper, L. H. N. (1938a). Salt crror in determinations of phosphate in sca water. J . mar. biol. Ass. U . K . 23, 171-178. Cooper, L. H. N. (1938b). Redefinition of the anomaly of thc nitrate-phosphate ratio. J. mar. biol. Ass. U . K . 23, 179. Cooper, L. H. N. (1939). Phosphorus, nitrogen, iron and manganese in marine Zooplankton. J. mar. biol. Ass. U . K . 23, 387-390. Corner, E. D. S. (1961). On the nutrition and metabolism of zooplankton. I. Preliminary observations on thc fecding of the marine copepod, Calanus helgolandicita (Claus). J . mar. biol. Ass. U . K . 41, 5-16. Corner, E. D. S. and Cowey, C. B. (1964). Somc nitrogenous constituents of the plankton. Oceanogr. Mar. Bwl. Ann. Rev. 2, 147-167. Corner, E. D. S. and Cowcy, C. B. (1968). Biochemical studies on tho production of marino zooplankton. B i d . Rev. 43, 393-426. Corncr, E. D. S., Cowey, C. B. and Marshall, S. M. (1965). On the nutrition and metabolism of zooplankton. 111. Nitrogen excretion by Calanua. J. mar. b i d . Ass. U . K . 45, 429-442. Corncr, E. D. S.. Cowey, C. B. and Marshall, S. M. (1967). On the nutrition and metabolism of zooplankton. V. Feeding efficiency of Calanua finmarchicua. J. mar. biol. Ass. U.K.41, 259-270.

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Corner, E. D. S. and Newell, B. S. (1967). On the nutrition and mctabolisrn of zooplankton. IV. The forms of nitrogen cxcreted by Calanue. J. mar. biol. AIM.U . K . 47, 113-120. Cowey, C. B. and Corner, E. D. S. (1963a). Amino acids and some other nitrogenous compounds in Ca2anus jinmarchicus. J. mar. biol. Aea. U . K . 43, 485-493.

Cowey, C. B. and Corner, E. D. S. (1963b). On tho nutrition and mctabolisrn of zooplankton. 11. Tho relationship between the marine copepod Calanus helgolandicua and particulate material in Plymouth sea watcr, in tcrms of amino acid composition. J . mar. biol. Ass. U.K. 43. 495-511. Cowey, C. B. and Corner, E. D. S. (1966). The amino acid composition of certain unicollular algae and of the faecal pellets produced by Culunus jinmarchicus when feeding on them. In “ Some Contemporary Studies in Marine Science ” (H. Barnes, ed.), pp. 225-231. Georgo Allen and Unwin, London. Craig, H. and Gordon, L. I. (1963). Nitrous oxide in tho ocean and the marine atmosphere. Geochim. coemochim. Acta, 27, 949-955. Curl, H. Jr. (1962). Standing crops of carbon, nitrogen, and phosphorus and transfer bctween trophic levels in Continental Shelf watcrs south of New York. Rapp. P.-v. Rdun. Cons. perm. int. Explm. Mer, 153, 183-189. navies, A. G. (1970). Iron, chelation and the growth of marine phytoplankton. I. Growth kinotics and chlorophyll production in cultures of tho euryhaline flagellato Dunaliella tertiolech under iron-limiting conditions. J. mar. bwl. A88.

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Delff, C. (1912). Beitrage zur Kenntnis der chemischen Zusammcnsctzung wirbelloser Meerestiero. Wise. Meereauntere. Abt. Kiel, N.F. 14, 51-81. Dresel, E. I. B. and Moylc, V. (1950). Nitrogenous exrrction of amphipods and isopods. J. exp. Bwl. 27, 210-225. Droop, M. R. (1968). Vitamin B12and marine ecology. IV. Tho kinetics of uptake, growth and inhibition in Monochryeia lutheri. J. mar. bwl. Aee. U . K . 48, 689-733.

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Dugdale, R. C., Menzel, D. W. and Ryther, J. H. (1961). Nitrogen fixation in the Sargasso Sea. Deep-sea Rea. 7 , 297-300. Edmondson, W. T.. Comita, G. W. and Anderson, G. C. (1962). Kcproductive rate of copepods in nature and its relation to phytoplankton population. Ecology, 43, 625-634. El-Sayed, S. Z. (1970). On the productivity of the Southern Ocean (Atlantic and Pacific sectors). In “Antarctic Ecology ” (M. W. Holdgate, ed.), vol. I.

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Eppley, R. W. and Coatsworth, J. L. (1968). Uptake of nitrate by Ditylum brightwellii-Kinetics and mechanisms. J. Phycol. 4, 151-156. Eppley, R. W. and Thomas, W. H. (1969). Comparison of half-saturation constants for growth and nitrate uptako of marine phytoplankton. J. Phywl. 5, 375-379. Eppley, R. W., Coatsworth, J. L. and Sol6rzan0, L. (1969a). Studies of nitrate reductaso in marine phytoplankton. Limnol. Oceanogr. 14, 194-205. Eppley, R.W., Rogers, J. N. and McCarthy, J. J. (1969b). Half saturation constants for uptake of nitrate and ammonium by marine phytoplankton. Limnol. Oceanogr. 14,912-920. Ferrara, R. (1953). Phytoplankton studies in uppor Narragansett Bay. M.S. Thesis, University of Rhode Island. Fiadeiro, M., Sol6nan0, L. and Strickland, J. D. H. (1967). Hydroxylamine in sca water. Limnol. Oceanogr. 12, 555-556. Fleming, R. H. (1940). The composition of plankton and units for rcporting populations and production. Proc. 6th Pac. Sci. Congr. 1939, 3, 535-540. Fogg, G. E. and Than-tun. (1958). Photochemical rcduction of elementary nitrogon in the blue-green alga Anabaenu cylindriea. Biochim. biophys. Acta, 30, 209-210. Fraser, J. H. (1969). Experimental feeding of some medusae and Chactognatha. J. Fish. Rea. Bd Can. 26, 1743-1762. Gardiner, A. C. (1937). Phosphate production by planktonic animals. J. Cone. perm. int. Explor. Mer, 12, 144-146. Geen, G. H. (1965). Primary production in Bras d’Or Lake and other inland waters of Cape Breton Island, Nova Scotia. PhD Thesis, Dalhousio University, Halifax, Nova Scotia. 187 pp. Gerking, S. D. (1962). Production and food utilization in a population of Bluegill Sunfish. Ewl. Monogr. 32, 31-78. Goering, J. J., Dugdale, R. C. and Menzel, D. W. (1966). Estimates of i n Bitu rates of nitrogen uptake by Trichodesmium sp. in tho tropical Atlantic Ocean. Limnol. Oceanogr. 11, 614-620. Goldberg, E. D., Walker, T. J. and Whisonand, A. (1951). Phosphate utilization by diatoms. Bwl. Bull. mar. bwl. Lab.,Woods Hole, 101, 274-284. Grainger, E. H.(1959).The annual oceanographic cyclo at Igloolik in the Canadian Arctic. I. The Zooplankton and physical and chemical observations. J. Fish. Rea. Bd Can. 16, 453-501. Grant, B. R. (1967). Tho action of light on nitrate and nitrito assimilation by the marine chlorophyte Dunaliella tertiolectu Butcher. J. gen. Microbwl. 48,379-389. Grant, B. R., Madgwick, J. and DalPont, G. (1967). Growth of Cylidrotheca closterium var Calijornica (Mereschk)Roimann & Lowin on nit,rate, ammonia and urea. Aust. J. mar. Freshwater Res. 18, 129-136. Grill, E. V. and Richards, F. A. (1964).Nutrient regeneration from phytoplankton decomposing in seawater. J. mar. Rea. 22, 51-69. Guillard, R. R. L. (1963). Organic sources of nitrogen for marine centric diatoms. I n “ Symposium on Marine Microbiology ” (C. H. Oppenhcimer, ed.), pp. 93-104. Charles C. Thomas, Springfield, Illinois, U.S.A. Hamilton, R. D. (1964). Photochemical processes in tho inorganic nitrogen cycle of the sea. Limnol. Oceanogr. 9, 107-111. Hansen, A. L. and Robinson, R. J. (1953). The determination of organic phosphorus in ma water with perehloric acid oxidation. J. mar. Rea. 12, 31-42.

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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

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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

u<;ft!hhm'&, \%3

TAURINE

IN MARINE

INVERTEBRATES

213

Thus apart from the occurrence as a conjugent with cholic acid in bile salts of vertebrates, taurine occurs widely in invertebrates-particularly marine invertebrates, in its free form. The taurine content of the different tissues of any animal varies but it may be in concentrations greater than other amino acids (Tables IV, V, VI and VIII). Although this is open to dispate (Degens, 1967), Kittredge et al. (1962) found little phylogenctic correlation of amino acid patterns in invertebrates and found that this is apparently true also of the distribution of taurine. TABLEIv. THEPROPORTIONS OF THE INDIVIDUAL AniINo ACIDSI N ETHANOLIC EXTRACTS OF LOBSTER MUSCLE(From Kcrmack et al., 1955). Each figure is basod on values obtainod from tho analysis of extracts of twoor more lobstors.

Amount

Amino acid

Alanine Arginine Aspartic acid Glutamic acid Glutamine Glycine Histidine Loucine Lysino Proline Serine Taurino Thrconine Tyrosine Valine

(ae yo of total -amino N ) 5.1 5-7

Trace 0-8 6.2 21.9 0.5 4.1 2.3 37.3

2.2 10.1

0.6 0.9

. 6.0

Thus in the polychaete Audouinia fresh body wall muscle contains more than 3% tnurine whereas that of Nereis and Glycera contains little or none, although the amino-nitrogen content of these worms is almost identical. I n molluscs taurine is present in marine and brackish water forms sometimes in very large quantities (Tables I and II), but in terrestrial and freshwater species it is absent (Simpson et al., 1959) but not necessarily because the latter are unable t o synthesize the substance (Allen and Awapara, 1960). As will be shown later, there are probably physiological reasons for this difference (page 232). I n

214

J. A. AILEN AND M. R. GARRETT

vertebrates* (but still t o be confirmed in invertebrates) the taurine concentration in tissue may be constant, even when its synthesis is reduced, for example, by vitamin B, deficiency (Hope, 1957). It is present in the greatest quantities in tissues having the greatest metabolic activity, vide heart and muscle, and is held there against a large concentration gradient. TABLEV. THE AMINOACIDSPRESENT IN AQUEOUS EXTRACTS OF MUSCLEAND HEPATOPANCREAS (From Kermack et al., 1955). The relative abundance was estimated from visual inspection of the SpOtSona two-dimensional chromatogram. - Indicates not detected.

Amino acid Muscle Proline Glycine Taurine Alanine Arginine Glutamine Leucine Valine Glutamic acid Lysine Serine Tyrosine Histidine Threonine Aspartic acid

+++++ +++++ ++++ +++ +++ +++ +++ +++ ++ ++ ++ ++ + + Trace

Relalive abundance Hepatopancreaa

Blood

++ +++++++ +++++ ++ -

+ + -

+

-

-

+

It is unfortunate that its function as an emulsifier of fats when in conjugation with cholic acid, and that it is an end product of sulphur amino acid metabolism, has obscured other and equally important functions. This conclusion is high-lighted by the invertebrates where, although it appears t o play no part in fat digestion, in many marine *There is a recent, and very fine, review by Jacobsen and Smith (1968) of the extensive literature concerning taurine in vertebrates, including man. This also gives details of methods of estimating taurine and the physical properties of it and related compounds. Therefore, in the present review, reference to work on vertebrates is given for comparative purposes and where it is essential to the discussion of work on marine invertebrates. While the review by Jacobsen and Smith (1968) includes sections on invertebrates, it does not deal with them in any great depth, nor does it cover all the literature. Its main content is mammalian function and the relation of taurine to various clinical conditions in man.

TAURINE IN MhRINE INVERTEBRATES

216

species it occurs in large quantities. Thus the purpose of this review is to assess and discuss what little is known of its occurrence and functions in invertebrates in the hope that it might stimulate research into the functions of one of the more neglected chemicals commonly present in tissues of these animals. TABLE VI. THEDISTRIBUTION OF TAURINE IN Mytilw, edulie (From Lange, 1963). Organ

Total body Gill Foot Muscle Mantle Haemolymph* Pericardial fluid?

t

g taUrine/lOO g wet tissue

0.68 0-4 0.7 0.9 0.5

0.03 0.00

Haemolymph was obtained by bleeding the animals. Pericardial fluid waa obtained by a syringe from the pericardial cavity.

11. CHEMISTRY Most of the investigations into the formation of taurine in animals have been carried out on vertebrates and on the rat in particular. Methionine is usually consideredto be the starting point in the formation of taurine (Fig. l), thus Tabachnick and Tarver (1955) injected S35 methionine into rats and recorded labelled cystathionine, cysteic acid and taurine in the liver. Medes and Floyd (1942) and Chapville and Fromagcot (1955) found that taurine could be formed from cystine in the liver and they and Blaschko (1942) later found a decarboxylating enzyme for converting cysteic acid t o taurine both in the liver and in the kidney of the rat. Awapara et al. (1950), demonstrated that following the injection of cysteine* into rats there was an increase of taurine in the liver, together with a corresponding increase in alanine. In earlier studies the insoluble portion of rat liver homogenates was used in the catalysis by cysteine oxidase of cysteine to cysteine sulphinic acid. The catalytic activity was low, and the supernatent was later shown to be more active than the insoluble fraction (De Marco et al.,1966; Sorb0 and Ewetz, 1965; Wainer, 1965). Curiously, cysteine oxidase is apparently not present in the brain (Wainer, 1965) even Cystine and cystcine are interconvertible, although the rate and nature of the conversion are not fully understood (Baldwin, 1962).

Methimine /- Swine

Hornocystine

- 1

Homocysteine

Cvstothionine

_ _ _ _ _ _ _ _ _ _ _ _ _ _ _ _ _ _ -----------+ Cystine *-*

_. Cysteine

_ c - * * iCHZSH ~2~~~~ I

I

CHNHZ CHNHZ I 1 COOH COOH

**-* ****

-

/ /’

CHNH2 I COOH

Cysteornine

I

t

---

Cyrtamincd,sulphoaid~ 5.

I

!

FIG.1. Metabolic pathways associatod with taurine.

TAURINE I N MARINE INVERTEBRATES

217

though cysteine sulphinic acid is known t o be present and that the latter can be formed from S35 methionine (Bergeret and Chatagner, 1954; Peck and Awapara, 1966). This is also true of rat heart and it must be concluded that another pathway is present in these tissues (see below). Fromageot et al. (1948) showed that under anaerobic conditions, cysteine sulphinic acid in the presence of rabbit liver extract gave rise to alanine and sulphite by desulphination. This work was followed by further experiments by Chatagner and Bergeret (1951, 1955), Bergeret and Chatagner (1952,1954,1956) and Bergeret et al. (1952) in which, by increasing the amount of cysteine sulphinic acid in the above experiment followed by paper chromatographic separation, they found an additional and new neutral sulphur amino compound which they suggested was formed by decarboxylation of the cystcine sulphinic acid and which they named hypotaurine. COOH

I I

CH.NH,-

CH,.NH,

I

t co,

CH,.SO,H

CH3.S0,H CYSTEINE SULPHINIC ACID

HYPOTAURINE

This they confirmed manometrically and also showed that hypotaurine was produced in vivo in rats following injection of liver extract. of control rats previously injected with L-cysteine sulphinic acid. Furthermore, they found it was present in small amounts in the liver of normal animals. Bergeret and Chatagner (1952) and Bergeret et al., (1952) showed that both the formation of alanine and SO, and of hypotaurine from L-cysteine sulphinic acid was enzymatic. These observations are clearly related t o those of Awapara et al. (1950) when the latter found that alanine as well as taurine is formed in the liver after injection of cysteine. When Awapara (1953) and Awapara and Wingo (1953) repeated the earlier experiments they too found hypotaurine (2aminoethanesulphinic acid) in the liver of rats. Awapara (1953) suggests that the following two-step reaction takes place in the liver: Oxidation of cysteine to cysteine sulphinic acid and decarboxylation of the latter t o hypotaurine. I n addition Awapara and Wingo (1953) suggest that cysteic acid, which Medes and Floyd ( 1942) and Blaschko (1942) had found t o give taurine on decarboxylation, was not in fact the normal precursor, but that the above was the preferred pathway (Fig. 1). Furthermore, the results of the latter workers could be ex-

218

J. A. ALLEN AND M. R. GARRETT

plained in terms of the abnormally large doses used in experiments iu vilro. No cystcic acid was found in the liver of rats in injection experiments with small amounts of cysteine S3=. However, cysteic acid injected in large quantities results in the formation of taurine. Thus the organism may be capable of oxidizing eysteine to cysteic acid and then decnrboxylnting tlic latter to taurine but only as an alternative pathway. Awapara and Wingo ( 1 983) assume that taurinc! is formed froin hypotaurinc by oxid.dt'1011. The resiilts of Blaschko et al. (1963) a t first sccmcd to contradict the theory that the normal pathway from cysteine to taurine is via the intermediate hypotaurine when they found that pyridoxine* deficient rats did not excrete tauriiie (although this was proved later not to be a total loss) and at the same time thcy could find no cvidencc of cysteic acid decarboxylase activity in the liver. Yet Fromageot (1951), who found that in Vitamin B,* deficiency taurine and hypotaurine are absent from urine, also demonstrated in vitro that decarboxylation of cysteine sulphinic acid had been suppressed. This was latcr confirmed by Chatagner et al. (1964). To explain the apparent discrepancy of the previous results, Blasehko and Hopc (1954) repeated the suggestion of Awapara and IVingo (1953) that some pyridoxine " requiring " enzyme is responsible both for the decarboxylation of cysteie acid and of cysteinc sulphinic acid. Strong support for this view came when Hope (1956) found that liver extract from dogs, rats and other mammals could decarboxylate both L-cystcic acid and L-cysteine sulphiiiic acid although the rate of decarboxylation of thc sulphinic acid was greatcr than tlie cysteie acid. However, high decarboxylation activity with one substrate was always linked with high activity in the other and in animals such as thc cat where thcrc is no decarboxylation of ~-cysteic acid, there is no drcarboxylation of L-cystehe sulphinic acid either. While the rcsults explain why L-cysteic acid can act as a.precursor of tauriiie, it seems likcly that r,-cysteine sulphinic acid is the chicf substrate for the enzyme, and is the preferred pathway for taurine formation. Bergerct et al. (1958) and Jacobsen et al. (1964) found that the decarboxylase of tlie brain of the rat differed from that of the liver. Brain decarboxylasc is unaffected by Vitamin Be deficiency while that of the liver is entirely suppressed. Hope (1957) similarly found the amount of taurine in the brain to be unaffected by pyridoxine deficiency Pyridoxal phosphate, cofactor in decarboxylaso activity, is the prccursor of pyridoxine. Vitamin B, comprisos a family of substances structurally rolated to pyridoxal phosphate and presumably Ba doficiency has the same effect as pyridoxine deficiency (see Jacobsen and Smith, 1968).

219

TAURINE IN MARINE INVERTEBRATES

although taurine in the liver was lost. However, to act, brain decarboxylase requires pyridoxine (Davison, 1956 ; Jacobsen and Smith, 1963; Jacobsen et al., 1964). The presence of this brain isoenzyme explains why taurine is not completely absent from urine in pyridoxine deficient animals as had been thought previously (Blaschko et al., 1953) but continues to be excreted in small quantities. The oxidation of hypotaurine t o taurine was first demonstrated by Cavallini et al. (1954) when they injected rats with hypotaurine. They were unable to show this in vitro using a homogenate of rat organs. Eldjarn and Sverdrup (1955) and Eldjarn et al. (1956) confirmed these experiments when they found that following the injection of hypotaurine S35into the rat they could recover most of the radioactivity in the urine as sulphate and taurine. The oxidation of hypotsurineto taurine is very rapid and labelled taurine exceeding the amount of labelled hypotaurine in the body is present in urine 30 minutes after injection. The formation of sulphate from taurine is probably very limited in the rat and the formation of sulphate from hypotaurine is via another reaction. Work on taurine formation in marine invertebrates appears to show the same pathways that are present in vertebrates. Abbott and Awapara (1960) working with Arenicola cristata and Simpson et al. (1959) and Allen (personal observations) working on M y a showed qualitatively that the intermediates found following the injection of labelled methionine and cysteine are the same as those in similar experiments with vertebrates (Table VII). Thus it is suggested that taurine is formed from methionine or cysteine via decarboxylation of cysteine sulphinic TABLE VII. EXPERIMENTS INVOLVING THE INJECTION OF LABELLED COMPOUNDS INTO Arenicola cri.&z!u (Extracted from Abbott and Awapara, 1960).

Subetunce injected Compound found to be radioactive Sulphate Homocysteine Cystathiono Cysteine Cysteinesulphinic acid Hypotaurine Taurine

536

536

3C"

taurine

methionine

cyeteine

cyetine

eehne

+ + + + +

+ + +

+ +

+

+ + + + + + +

+

+

535

d36

220

J. A. ALLEN AND M. R. GARRETT

acid to hypotaurine with subsequent oxidation of the latter. Thoai et al. (1963) also reported the conversion of S35cysteine to hypotaurine in Areiticolu, but they did not say whether radioactive cysteine sulphinic acid or cysteic acid were present. It should. be noted that Robin and Roche (1954) investigated several coelenterates and sponges and observed that taurine and hypotaurine always occur together. Shibuya and Ouchi (1957) found hypotaurine in every tissue of the mollusc Septifer and it has been reported from other molluscs (Ouchi 1959, Tanaka, 1960). Awapara (1962) was able to oxidize hypotaurine t o taurine i n vitro using fresh whole homogenates and soluble enzyme extracts of Arenicola cristnta. However, the reaction appeared t o be non-enzymatic as it was not hindered by prolonged boiling and although the presence of worm homogenate or extract was necessary for the reaction they suggest a metal ion may be acting as the catalyst. Earlier, Schoberl (1933) had suggested that the conversion of cysteine t o taurine might be by way of cystamine. The existence of another route to hypotaurine from cysteine or cystine was again suggested by Eldjarn (1954a and b) and Eldjarn and Pihl (1956) and by Cavallini (1966) and Cavallini et al. (1955) when they found more hypotaurine in the urine of the rat after feeding or injecting cystine or cysteine, than if cysteine sulphinic acid was fed or injected. Thus, although cystcine sulphinic acid is generally accepted as a precursor of hypotaurine they found that it was only converted in part t o hypotaurine. These authors also found cystamine disulphoxide in the urine of rats fed cystine. Although this is known to be a product of hypotaurine under certain conditions, they suggested, as did Medes and Floyd (1942), that it too might be an intermediate in the cystine-hypotaurine pathway. Eventually, Cavallini et al. (1963, 1966) showed that an alternative enzymatic pathway does exist. The purified enzyme showed specificity towards cystamine, and under conditions in which the latter substance is oxidized to hypotaurine, cysteine and cystine derivatives are not oxidized t o a level higher than that of a disulphide. The authors are of the opinion that cystamine (and cysteamine) could be the preferential intermediates compared with cysteine sulphinic acid in the route from cystine to hypotaurine and taurine, particularly as it has been shown that this enzyme is widespread in animal tissues (DuprB and De Marco, 1964). In fact, DuprB and Dc Marco (1964) also had predicted this pathway. The presence of thiotaurine in the urine of rats fed with L-cysteine also gives indirect evidence of this pathway (Cavallini et al., 1959, 1960; Mondovi and Tentori, 1961). The conversion of cystamine t o hypo-

22 1

TAURINE IN MARINE INVERTEBRATES

taurine is thought to involve oxidation and deamination of cysteine t o cystaldimine followed by the degradation of the latter to thiocysteamine which spontaneously breaks down to cysteamine and sulphur. Cysteamine on oxidation is then converted to hypotaurine, some of which is transsulphurated to thiotaurine (Jacobsen and Smith, 1968). Cysteamine is also thought t o be derived from cysteine via coenzyme A (Fig. 1). TABLEVIII. ESTIMATED CONCENTRATIONS OF SIX AMINO ACIDSI N TISSUESOF MARINEINVERTEBRATES Figures estimated from histograms givon by Simpson et al. (1959). p

Species

Bunodoaoma covernata Penaeua aztecw, Clibanariua vittatw, Pagurw, pollimris Siphonaria lineolata Fmciolaria dietuna Bu.ycon peruersurn Thak haemaatoma Polynices duplicata Oliva aagana Lithophaga biaulcda Craaaoatrea virginica Arm umbonata Volsella demiaaua Loliguncula brevie Thyone sp. Luidia elathrata

&l aminolg tiasue

Alanine

Arginine

Glycine

1.0 5-2 4-0 7.0 5.5 2.0 4.0 7-4 18.0 2-3 0.8 7-0 5.0 12.0 15-0

1.0 6.5 4.0 4.5 1.4 2.0 3.0 4.5 3.0 1.0 1.0 1.0 1.5 1.0 1-4 0.5 0.4

3.0 56.0 6.0 23-0 2.4 5.0 2.5

5-0

20.0 8-0 1.0 14.0 6.3 6.0 11.5 20.0

34.0

Glutamic 1.0 2.0 2.8 2.4 3.0 2.3 1.2 1.0 1.5 1.5

-

5.5 6.0 2.2 2.0 14.0 2.5

AaparTaurine tic 0.8 0.8 0.5 0.3 1.2 1.5 2.0 3.0 2.3 0.5 1.4 1.5 2.5 1.2

0.6 2.0 2-6

10.0 23.0 2-4 36.0 4.3 12.0 15.0 16.0 60.0 5.6 11.0 6.0 70.0 10.0 55.0 20.0 11.0

The work of Yoneda (1967) on Mytitus adductor muscle-known t o contain large quantities of taurine (page 215) indicated that this pathway might also exist in invertebrates. He incubated cysteine and cysteamine with enzyme extracts of adductor muscle and showed that cysteamine was metabolized to a greater extent than cysteine, but a t this stage did not identify the products. Further studies (Yoneda, 1968) showed that during the incubation of cysteamine with Mytilus adductor muscle extract small amounts of hypotauriiie were formed, although 30% of the cysteamine was converted to taurine within two hours. When hypotaurine was incubated with the same mixture an increase in taurine was recorded. Yoneda (1968) concluded that there must be a

222

J. A. G E N AND Y.R. GARRETT

new enzyme or enzyme system present that catalyses the oxidation of cysteamine to taurine directly and not via hypotaurine. This is not necessarily significant if oxidation is non-enzymatic (Abbott and Awapara, 1960). Other authors have failed to convert hypotauriiie to taurine in vitro (Jacobsen and Smith, 1968). Allen and Awapara (1960) showed that Rangia cuneuta Gray, a freshwater bivalve normally containing no taurine, could synthesize taurine from injected S35methionine via the oxidation of cysteine sulphinic acid to cysteic acid followed by decarboxylation of the latter to form taurine and with some production of labelled sulphate. Taurine is excreted by Rangia as soon as it is formed. Note, this sequence is regarded as a secondary pathway in vertebrates. In parallel experiments using Nytilus edulis LinnB, they found 24 h after the injection of S35 methioniiie, labelled hypotaurine and taurine to be present, but only in small quantities. Formation of taurine in this animal, which normally contains large amounts of the substance, is a slow process. In addition, in the Mytilus experiments, Allen and Awapara (1960) recorded labelled cystathionine, an unknown compound which they thought possibly to be methionine sulphate, together with a relatively small amount of cystine/cysteine. These additional results together with those obtained invitro by Yoneda (1968) indicate that the pathway via cysteamine suggested by Cavallini et al. (1955) may exist in Mytilus. However, the fact that in experiments using cysteamine, taurine formation i n vivo is a slow process (much slower than found i n vitro) and that cysteamine is not readily identified as being present in the animal suggests that it is more likely that cysteine sulphinic acid is the intermediate, and that the low rate of taurine synthesis in Mytilus prevented Allen and Awapara (1960) from identifying it. Curiously in Mya, injected S35methionine is metabolized at a very high rate. There is a high yield of taurine, up to 50% of recovered activity, within the first hour. The taurine is also subject to a high rate of turnover, 50% being converted to other substances within 15 h (Allen, personal observations). There is some evidence that other pathways may exist for the formation of taurine. Thus, sulphate sulphur may be incoporated into taurine. Jacobsen and Smith (1968) point out that xenic cockroaches possess all the necessary chemical steps. Bostr6m and Aqvist (1952) injected rats interperitoneally with the sodium sulphate labelled with S35 and isolated labelled taurine from the liver after 2 h and recorded the maximum concentrations after 8 h. In addition very small amounts of labelled methionine and cystine were found in the liver after 24 h. This was confirmed by Dziewiatkowski (1954) who, however, believed

TAURINE IN MARINE INVERTEBRATES

223

that cystine was formed by bacteria in the gut. Machlin el al. (1953) administered S35labelled sulphate to hens and recovered labelled cystine from their eggs, methionine remaining unlabelled. Machin et al. (1955) later injected S35labelled sulphate into chick embryos and found that all the S35bound in organic material was incorporated into taurine. Lowe and Roberts (1966) repeated this work with a similar result, cystine, cysteic acid and methionine remaining unlabelled. Their chromatograms also showed the formation of a possible precursor of taurine. This did not react with ninhydrin and they did not identify the substance. Yet another spot not reactive to ninhydrin appeared much later on their chromatograms and this they hint might possibly be 2-hydroxyethanesulphinic acid (isethionic acid) which Koechlin (1954a and b, 1955) had identified a year earlier as being present in large quantities in the axoplasm of the giant nerve fibres of squid. Martin et al. (1966) and Miraglia et al. (1966) kept chicks on a basal diet low in sulphate for 14 days and then added S35sulphate to their diet. The labelled sulphur became incorporated into taurine and taurocholate. On addition of inorganic sulphur compounds the proportion of radioactive sulphur incorporated into taurine increased, possibly indicating that there is an optimal substrate sulphur level. Addition of glycine to the basal diet also gave an increased rate of taurinc synthesis. Methionine, cystine or cysteic acid showed little radioactivity. Following the accumulation of labelled taurine in the liver there was an increase in a substance which had the same Rf value as isothionic acid. Chick liver, heart, spleen and kidney can actively convert taurine to this acid. Under some dietary conditions a spot was found on the chromatograms having an Rf value of mercaptoethylamine and another of lesser activity identified with hypotaurine. Martin et al. (1966) suggest that, as in some bacteria, the formation of taurine from sulphate may be mediated by the cysteine level and involve enzyme repression or feedback, which might suggest that cysteine could be formed from taurine. All the above experiments indicate that vertebrates readily synthesize taurine using inorganic sulphate sulphur. Jacobsen and Smith (1968) suggest that the conversion of inorganic sulphate to taurine is carried out in three stages : (1) the reduction of sulphate to sulphite ; (2) the fixation of sulphite to a 3 carbon aminated molecule derived from L-cysteine leading to the formation of L-cysteic acid (the enzyme involved, cysteinelyase, requires pyridoxine and probably breaks the CS bond of the 8-carbon of cysteine with the formation of an intermediate, possibly a-aminoacrylic acid) ; (3) the decarboxylation of cysteic acid t o form taurine. This pathway may be restricted to the

224

J. A. ALLEN AND M. R. GARRETT

chick embryo and incorporation of sulphate t o taurine in other animals may be by another pathway. The pathway(s) does not seem t o involve other sulphur amino acids. Thus, mercaptoethylamine may be synthesized separately or as part of the sulphate-taurinc pathway. It also seems possible that this may be the substance that Lowe and Roberts (1955) failed t o identify. It should be also noted that mercaptans are present in some polychaetes, notably Travisia. Until the work of Lowe and Roberts (1955) and Martin et al. (1966) demonst,rated the formation of isethionic acid, taurine and sulphate ions had generally been considered the end products of sulphur metabolism and the forms in which sulphur is excreted. The formation of labelled isethionic acid has been shown t o occur when sliccs of dog heart are incubated with S35-taurinc (Read and Welty, 1962) and Peck and Awapara (1967) show that it is formed in the brain of the rat. Isethionic acid is the hydroxy analogue of taurine and the latter authors suggest that it is formed from taurine in two stages by transamination to 2-oxoethane sulphonic acid followed by reduction of aldehyde. Isethionic acid has been found in invertebrates. Large quantities are present in squid nerve fibre (almost 50y0 of the total anions) together with taurine (Koechlin, 1955). This was, in fact, the first record of isethionic acid in biological matcrial. Since then its presence in squid has been confirmed and observations on its distribution have been extended t o other molluscs, Deffner and Hafter (1959, 1960) and Deffner (1961). They also report that isethionic acid is lacking or, if present, is in low quantities in Crustacea. They report finding cysteic acid amide in squid nerves, which they think might have been formed from isethionic acid and urea (Deffiier and Hafter, 1959). Apart from the enzymatic deamination of taurine t o form isethionic acid (and in vertebrates its conjugation with cholic acid t o form taurocholic acid) taurine appears t o be the precursor of taurocyamine, carbamyltaurine, asterubin, taurobetaine and trimethyltaurine. Taurocyamine was first synthesized by Engel (1875) but it was not found in a living animal until 1953 when Thoai et al. (1953a and b) and Thoai and Robin (1954) found it in the polychaete Arenicola marina (Linnd). They also showed that it was present in Sabellaria alveolata (Linnd) and Clymene lumbricoides Quatrefages and in the sipunculid Phuscolosoma elongatum Keferstcin and since then in other sedentary polychaetes and sipunculids (Table I). It appears that while taurocyamine occurs in sedentary polychaetes, it is absent from errant species (Table I). Abbott and Awapara (1960) were unable t o detect radio-activity in taurocyamine following their injection experiments with Arenicola (see

TAURINE I N MARINE INVERTEBRATES

225

Ta.ble VII). However, by repeating the taurine S35injection with material of higher specific activity they were able to detect a slight amount of radioactive sulphur in taurocyamine after 12 h. I n one ease in the following experiments in vitro they were able t o show transamidination between arginine and taurine. 0.004 p mole of taurocyamine was recorded in a sample containing 100 p moles of arginine, 5 p moles of taurine and 0.61 g freshweight worm tissue. Taurocyamine is a guanidinc derivative (2-guanidocthanc-sulphonic acid) and its occurrence in Arenieola muscle together with the absence of any other guanidinc derivative, suggested that its function was, like that of any other guanidine derivative found in muscle, that of a P acceptor in muscular contraction. This theory is supported by the fact that its phosphagen (phosphotaurocyamine) was also found (Thoai et al., 1953a and b). This was later confirmed by Griffiths et al. (unpublished work quoted by Ennor and Morrison, 1958) who found the same phosphagen in Phuscolosoma moduliferum and ArenicolG assimilis Ehlers. Phosphotaurocyamine appears t o havc a more limited distribution than taurocyaminc. Curiously, taurocyamine has not been reported in adult Audouinia although it is so rich in taurine (Kurtz and Luck, 1935). However, it has been found in the egg (Robin et al., 1956).

-

/

NH

N

P03H1

HN = C

\

NH-CH,-CHZ-SO,H

NHa

+ ADP + HN = C / \

PHOSPHOTAUROCYAMINE

+ ATP

NH-CHZ-CHS-SO jH TAUROCYAMINE

The enzyme concerned in the above reaction, taurocyaminephosphokinase, was purified from Arenicola marina muscle by Thoai and Pradel, (1962a and b) and Thoai and Roche, (1960). The importance of phosphagens in biological activity stems from the fact that their free energy of hydrolysis is greater than that of ADP. However, the free energy of hydrolysis of phosphotaurocyaminc is less than that of phosphagens most commonly found in vertebrates and invertebrates, namely, phosphocreatine and phosphoarginine, and about equal to that of phosphoglycocyamine, another phosyhagcn also found in marine worms (Thoai et al., 1953a and b). Marine polychaetes in fact are unique as a group in possessing all four of these phosphagens. Thoai and Roche (1960) suggest that t o each type of muscle there should be adapted a phosphagen of appropriate thermodynamic potential, thus, phosphocreatine should be present in fast muscles and phosphotaurocyamine and phosphoglycocyamine in slow muscles, since the order

226

J. A. ALLEN AND M. R. GARRETT

of the thermodynamic potential is phosphocreatine > phosphoarginine > phosphotaurocyamine and phosphoglycocyamine. Taurocyamine is not restricted t o polychaetes and sipunculids. Thus, Robin and Roche (1954), investigating taurine and taurine derivatives in various sponges and coelenterates, found it in Hymeniacedon caruncula Bowerbank, Thetia lyncurium Linn6 and in Actinia equina Linn6. The same workers (Roche and Robin, 1954) had also shown phosphoarginine and phosphocreatine to be present in Hymeniacedon and Thetia respectively, but they did not find phosphotaurocyamine. The presence of taurocyamine and the absence of its phosphagen clearly require further confirmation, but should this be so then another function for taurocyamine must be found. A clue may lie in experiments of Thoai et al. (1954, 1956)on the rat. The latter authors found taurocyamine in the urine following the injection of taurine. They did not find taurocyamine in muscle, but creatine is known to be the guanidine derivative acting as N P acceptor. They suggest that aa taurocyamine, like guanidine derivatives in general, is not easily hydrolysed by enzymes, it may be a link in a cycle in which amino acid can be excreted, and ammonia eliminated in a non-toxic form (Fig. 1). The presence of taurocyamine in the urine of rats (and also man) has been confirmed by Schram and Crockaert (1957a and b). However, they found no significant increase in excretion of taurocyamine when taurine was injected into rats, nor was there any increase in the urine of another supposed intermediate in this cycle, carbamyltaurine (2-ureidoethanesulphonicacid), in the same experiments. However, when carbamyltaurine and taurocyamine were injected, these were quickly excreted, most within the following 24 hours. Curiously carbamyltaurine (see Table I) was found nearly a century ago by Salkowski (1872, 1873, 1876) in the urine of dogs following administration of taurine. Before taurocyamine had been found in nature Ackermann (1936) hypothesized that it should be an intermediate product between taurine and its dimethyl derivative, asterubin (dimethyl guanidinotaurine). Ackermann (1935) had found asterubin in two species of Asterias. Twenty years later, following the work of Thoai et al. (1953a and b), Ackermann (1955) confirmed the presence of taurocyamine in Areniwla, although he did not find asterubin, nor, surprisingly, taurine. Jeuniaux et al. (1962a and b) showed that Asterias contains large amounts of taurine, however, they suggest a role unconnected with that of the formation of asterubin (see p. 236). This does not preclude the possibility that Ackermann (1936) was correct and that because taurine and asterubin are both present, taurocyamine may also be

TIURINE IN MARINE INVERTEBRATES

227

present in Asterias but as yet undetected. The only proof that in invertebrates taurine gives rise to taurocyamine has been given by Abbott and Awapara (1960). Following the injection of high specific activity S35taurine into Areniwla they were able to detect after 12 h a slight amount of radioactivity in the taurocyamine. In vitro, and in one case, they showed transamidination between arginine and taurine with the formation of a small amount of taurocyamine (p. 225) Transamidination betwecn arginine and hypotaurine, giving hypotaurocyamine (2-guanidoethanesulphinicacid) with subsequent oxidation to taurocyamine has been shown to occur in Areniwla and Phaswlosoma (Thoai et a,!., 1963). I n Areniwla, transamidination occurs in the gut and oxidation in muscle, whereas in Phaswlosoma oxidation occurs in the gut but not in the muscle of the body wall. As a result, Areniwla muscle contains ten times as much taurocyamine as hypotaurocyamine, while the reverse is true of body wall muscle of Phscolosoma. The inability of the muscle of the body wall of Phaswlosoma to oxidize hypotaurocyamine is attributed to low external oxygen tension. Details of the enzymes involved in this pathway are given by Thoai, 1957; Thoai et al., 1963a and b; Thoai and Robin, 1965; Thoai and Pradel, 1962a and b ; Thoai and Roche, 1960; Kassab et al., 1965; Hobson and Rees, 1957 ; and Ennor and Morrison, 1958. The metabolic fate of taurocyamine is unknown. Little is known of the other two derivatives of taurine found in invertebrates, except that taurobetaine was originally identified in the sponge Geodia gigas (Ackermann and List, 1959a and b) and later in the cnidarian Briareum (Ciereszko et al., 1961) and that trimethyltaurine is also found in Geodia gigas (Ackermann and List, 1959a and b).

111. FUNCTION When taurine was discovered in the mammalian liver it was thought to be an excretory product from the breakdown of sulphur-containing acid in the bile. In fact, it was conjugated with eholic acid in the bile forming taurocholic acid. Haslewood and Wootton (1950) in a eomparative study of bile salts, found taurine to be a conjugate in the bile of teleosts, snakes and some mammals, In other mammals, glycine was the conjugate and sometimes both glycine and taurine occurred together. I n elasmobranchs and amphibia, sulphate is the conjugate. Bile salts facilitate the emulsification of fats and because of their ability to form water soluble complexes with fatty acids they help in the absorption of free fatty acids. Apparently taurine does not have this function in invertebrates, although Vonk (1960) claimed a bile

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J. A. ALLEN AND M. R. GARRETT

salt, possibly taurodeorycholic acid, to be present in the gastric juice of Eriocheir and Astacus. Work by Oord (1966) and Oord et a2. (1965) did not confirm this, but they did show that emulsifiers were present, and also taurine, in the gastric juice of Cancer. While they tentatively suggested that the emulsifiers are fatty acylsarcosyltaurines, this is by no means certain. Although taurine was found in marine invertebrates soon after it was discovered in vertebrates, e.g. oyster and cuttlefish (Valenciennes and Frbmy, 1855) for many years it was considered to be nothing more than an excretory end product of sulphur amino acid metabolism. Bear and Schmitt (1939) investigating the ionic balance of giant squid nerve axoplasm found that their determinations indicated a large anion deficit of 490 m eq and an osmotic deficit of 280-415 mM. They suggested that this deficit was balanced by a large quantity of organic ions of moderate atomic weight. Webb and Young (1940) confirmed the large anion and osmotic deficits and gave figures of 368 m eq and 735 mM respectively from their determinations of electrolytes of the giant nerve fibres of Loligo. They point out, as did Bear and Schmitt ( 1939) that bicarbonates, sulphates, phosphates, lactates and proteins acting as acids could hardly amount t o more than 1-20 m eq and thus some unknown anion(s) must be present in a concentration of at least 0.25 N. Webb and Young (1940) recalled that Kelly (1904) had found considerable quantities of taurine in Mytilus muscle (400 mM/kg) while TABLEIX. THEAPPROXIMATE DISTRIBUTION OF THE PRINCIPAL FREEAMINO AND IN Carcinus ACIDSIN THE NERVESOF SOMEMARINE INVERTEBRATES MUSCLE(Extracted from Lewis, 1952).

Specim

Tieeue

Carcinua m a e w Cancer p a g u m Maia s q u i d 0 Homarua vulgaria Palinurw, vulgaria Sepia oficinalia Loligo forb& Carcinua

Aspartic

Nerve Nerve Nerve Nerve Nerve Nerve Nerve MUSC~Q

Glutamic

acid

acid

+++

++ ++ + + + ++ ++

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

+++ +++

f

Ahnine Taurine Glycine

++ ++ ++ ++ f + + ++ ++ f ++ + ++ f + +++ ++ +++ f ++ +++ +++ +++

Probable concentrations in m-moles/kgwet weight of tissue are : = >75 ; = 30-90; = 16-35; f = 6-16; - = < 5. These ranges are approximate.

++

+

229

TAURINE IN MARINE INVERTEBRATES

Henze (1911) had found betaine in octopus muscle. They overlooked the fact that Henze (1904,1913 and 1914) had also found large amounts of taurine in Octopus. Semi-quantitative analyses of the amino acids of nerves of seven species of marine invertebrates showed that on average taurine was second in abundance only t o aspartic acid (Lewis, 1952) (Table IX). He also made some accurate determinations of amino acids in nerves of three given species (Table X). It appears that in those cases where the taurine content was low, i.e. Homurus, Maia and Palinurus, there were relatively large amounts of glycine. Lewis (1952) considers that aspartate and glutamate, which make up a large fraction TABLEX. THECONCENTRATIONS OF THE PRINCIPAL FREEAMINOACIDS I N THE NERVESOF SOME MARINEINVERTEBRATES (Extracted from Lowis, 1952). Carcinwr w b l e leg nerve Aspartic acid Glutamic acid Alaninc Taurine Glycine Anion total N o . of analyses No. of nervcs analysed

138 35 33 65 <5 173 16 9

f 4.5 f 1-5 f 3-5 f5 f 5

Sepia eingle axon

Homarua whole leg nerve

82 39 21 103 <5 122 10 10

112 25 33 c12 35 137 8 3

A l l values in m-molcs/kg wct weight of nerve, f S.E. All ten Sepia axons were obtained from three animals.

of the amino acid content of the nerve, balance about 40% of the cations, i.e., most of the potassium ions present. His final calculations showed a remaining anion deficit of about 10% of the total. Although alanine and taurine together form more than 10% of the total solutes, they did not figure in the anion-cation balance sheet because they have no significant cation-binding power. Lewis (1952) was unaware of the existence of isethionic acid. A second function suggested at about this time was that taurine probably plays an important part in regulating the intracellular osmotic pressure. Krogh (1939) was among the first t o suggest this having observed high concentrations in Mytilus, Pecten and Sepia. Thus, when for example Hill (1950) concludes that single axons of Sepia behave as almost perfect osmometers, it is clear that the main-

230

J. A. ALLEN AND M. R. GARRETT

tenance of internal osmotic pressure is important for the optimum functioning of the nerves. But for taurine and alanine, the osmotic deficit in Carcinus nerve would be considerable. Lewis (1952) showed that amino acids are a conspicuous group of electrolytes in crustacean and molluscan nerves-up to 20% of the dry weight of the nerveswhich exist in a free state in the axoplasm. As exemplified by the rat (Awapara et al., 1950), vertebrate tissue contains much lower concentrations of free amino acids, particularly the neutral ones alanine, glycine and taurine. However, the relative distributions between muscle and nerve in vertebrates when compared with invertebrates is closely similar. Thus Carcinus muscle contains large quantities of taurine in comparison with nerve (Table 9) and similarly rat muscle contains six times more taurine than rat brain (Awapara et al., 1950). The higher concentration of taurine in marine invertebrate excitable tissue is certainly in part explained in terms of the maintenance of a higher internal osmotic pressure. Apparent confirmation of this conclusion came when Koechlin (1955) found relatively high concentrations of taurine in squid axoplasm, but in fact the major anion appeared to be isethionic acid which accounted for nearly 50% of the total anions. The presence of both these substances in axoplasm was suggestive of a metabolic relationship (Koechlin, 1955) and later Welty et al. (1962) and Read and Welty (1962) were able t o demonstrate the conversion of taurine to isethionic acid in dog heart tissue, presumably by the agency of a deaminating enzyme. If this is so then taurine, as the amino analogue, is also concerned in ionic balance as well as osmotic balance. In chemical terms, taurine might form a cyclical structure by hydrogen bonding between the amino group and the hydroxyl of the sulphonic acid group and in this form it would have no charged groups and could not attract cations. If it were then deaminated to isethionic acid a charged group on the sulphonic acid would be released thus allowing it to act as a strong anion. I n the quantities that isethionic acid is found in squid axon such a reaction would have a profound effect on the membrane potential (Koechlin, 1955; Read and Welty, 1962); Welty (1963) thought that taurine and isethionic acid might be functioning in a feed back system regulating potassium efflux from cardiac cells and the excitability of cardiac tissue. A theoretical model implicating isethionic acid in the conductance changes occurring in the squid axon during excitation, has been proposed by Mullins (1959), although Robertson (1965) rejected the view that isethionic acid has any specific role. Returning to the theory that taurine is used in osmotic balance Kossel and Edlbacher (1915) earlier suggested that this might explain the large quantities of glycine and taurine present in the caeca and

TAURINE I N MARINE INVERTEBRATES

231

gonads of Astropecten aurantiacus Grey. I n fact, they were the first to observe that the presence of organic nitrogenous substances in a free state would be important in the osmotic regulation of marine invcrtebrates and that this might be particularly true for poikilosmotic animals. Kurtz and Luck (1935) found large quantities of taurine in the polychaete Audouinia. They extracted 6-22 g taurinelkg of fresh whole worms and over 3% in fresh body wall muscle. They correlated this with the black layer of sulphurous mud that occurs around the tubes of these worms. They noted that other polychaetes, Glycera and Nereis obtained only a few feet from the Audouinia and on the same occasion did not have the black deposit around them. Only Nereis gave taurine on analysis, and then only in trace quantities. Similarly, estimations on the tissues of the sipunculid Urechis caupo, Fisher and MacGinitie, the phoronid Phoronopsis harmeri Pixell, and Lumbricus all gave negative results. The authors appreciated the limitations of the extinction method they used, but determinations of the sulphur content of the " taurine fraction " indicate that it is impossible that taurine could be present in quantity in the species they examined except in the case of Audouinia. Kurtz and Luck (1935) also determined the totd non-protein nitrogen and amino nitrogen of Audouinia and Nereis and found that in both cases the quantities were of the same order and that taurine must constitute most of the amino nitrogen present in dudouinia. While they could offer no explanation for the difference they do point out that in addition t o any excretory function that might be ascribed to the taurine of Audouinia (note the sulphur deposits around the worm) the high concentration of taurine will make it important osmotically and they put forward the idea that it may act as a zwitter ion. As a zwitter ion it would give one ion per molecule at the isoelectric point, and two ions per molecule at a pH sufficiently removed from it. In the latter case an amount of taurine as large as the 3% found in Audouinia would give a high enough osmotic pressure to balance a large proportion of the osmotic pressure of the surrounding aea water. Kurtz and Luck (1935) commented on the fact that at that time large amounts of taurine had only been found in marine animals. This has indeed proved true. Thus Simpson et al. (1959) determined the free amino acid content of seventeen marine invertebrates and found taurine in all varying from 2 pM/g tissue to 70 pM/g tissue. Because taurine content appeared t o vary with the environment they extended their analyses to land, freshwater and brackish water molluscs and found none in freshwater and terrestrial species but found taurine in brackish and marine species (Table VIII). They point out that the

232

J . A. ALLEN AND M. R. GARRETT

presence of taurine can be detectable a t concentrations as low rn 0.1 pM/g by their chromatographic technique. These results would again support the theory of taurine having an osmotic role. This work gave no inforniation as t o whether sulphur amino acids are metabolized differently in marine molluscs as compared with freshwater molluscs. However, Allen and Awapara (1960) carried out a number of experiments t d this end using Jlytilus edulis as an example of a marine mollusc and Rangia cuneata as the freshwater species. Their experiments showed that both can convert methionine t o cysteinc which in its turn can be oxidized to cysteine sulphinic acid and which can give rise to taurine and sulphate. Thus after injection of S35methionine t o both species, Mytilus edulis, known to contain large quantities of taurine, after 24 h contained labelled cystathione, an unknown which was possibly methionine sulphate, hypotaurine, taurine and sulphate, and a fairly small amount of cysteine/cystine while Rangia cuneata, which normally contains no taurine, had labelled cysteic acid and cysteine sulphinic acid (not found in Mytilus) but no cystathione or hypotaurine, yet larger quantities of cysteinelcystine than in Mytilus. Labelled taurine and sulphate were also present and in greater quantities than Mytilus. In repeat experiments, analyses a t different times up to 24 h after administration of S35methionine showed that in Rangia taurine is quickly formed (within 5 h) but is not held and has largely disappeared after 24 h. In the case of Mytilus the high concentration of endogenous taurine makes it difficult t o establish the rate of taurine formation. The significant difference between the two animals is the rate at which taurine is disposed of; thus, Mytilus keeps it by an unknown mechanism against a concentration gradient, while Rangia cannot hold the taurine it produces. If there are any differences in the metabolism of sulphur amino acids in the molluscs studied, the differences are in the intermediates, thus in Rangia taurine is probably formed mainly by decarboxylation of cysteic acid whereas in Mytilus it is mainly formed by oxidation of hypotaurine (Fig. 1). Potts (1958) also compared the adaptation of marine and freshwater bivalves to different external concentrations. He found that the amino acids contribute in major part t o the level of osmotic pressure in Mytilus. He found, too, that in Mytilus adapted t o half salinity that the amino acid and taurine content of the adductor and byssus retractor muscles was much reduced. However, in Anodonta amino acids play little part in the maintenance of its lower osmotic pressure, instead here potassium and phosphate ions make up the major contribution. Taurine is absent in Anodonta. In both Anodonta and Mytilus, adaptation to a changed osmolar concentration is brought about partly by water movement into

TAURINE IN MARINE INVERTEBRATES

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or out of the muscle fibres and partly by the increase or decrease of the total content of sodium, chloride and free amino acids in the muscles. Similarly Lynch and Wood (1966) in experiments on Crassostrea showed that with increasing environmental salinity the concentration of taurine in the body increased, as did that also of glycine, alanine and proline. Pctersen and nuerr (1969)did not find any direct relationship in the case of the prosobranch Tegula, rather the reverse. However, they report a direct relationship with a n unidentified compound, which could possibly be isethionic acid. Clearly these experiments should be repeated. Surveys on the amino acid content of marine, brackish- and freshwater crustaceans have shown that amino acid concentrations are greater in muscle of marine species than in that of freshwater species, in both cases the amino acid concentration of the blood is low in comparison with muscle (Camien et al., 1951). Duchiiteau and Florkin (1955)found that in Eriocheir there was little difference in the proportions of the different amino acids of the pool a t different salinities but that the concentration of all constituent amino acids was greater in sea water than in fresh water. They (DuchAteau and Florkin, 1956)found that this was also true of Carcinus maenas. They also refer t o both these decapods as being " poikilosmotic when in fact these animals exhibit some maintenance of the osmotic pressure of the blood thus buffering the effect of the external medium on the cells. The regulation of the cell volume and of the total number of moles of intracellular solutes-later termed isosmotic intracellular regulation by Jeuniaux et a2. (196l)-involves the constituent amino acids. They effect the opposition t o the movement of water between the cells and the internal medium which would otherwise result from the variations in concentration of the latter. Thus in marine invertebrates the concentration of certain amino acids and taurine in cells often exceeds that in the extracellular body fluid by several magnitudes (Florkin, 1963; Lange, 1965, 1968). The maintenance of this high concentration indicates that mechanisms exist for the active transport of taurine against covsiderable gradients. It apparently enters the cell in part by active transport at a specific site for amino acids, in part by active transport a t a less well defined site and in part by simple diffusion (Christensen, 1964;Christensen et al., 1954;Kromphardt, 1963). The concentration of amino acids and taurine in the cells is in part dependant on the osmolarity of the surrounding fluid, but it appears that any change is related only t o a small extent t o an apparent change in hydration of the tissues (Jeaniaux et al., 1961 ; Bricteux-Grbgoire et al., 1962, 1964s and b ; Lange, 1968). Lange (1963, 1968) points out that in Mytilus, ))

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taurine concentration increased relatively more than other amino acids with increasing salinity and thereby it exerts a sparing effect on the use of essential amino acids in osmoregulation. However, the role of taurine in this respect is not true of all marine animals. Jeuniaux et al. (196lb) in a study of the euryhaline carideans Palaemon elegans Rathke (Leader squiElu) and P . ( L . ) serrutus (Pennant) and their adaptation to brackish water (30% sea water) showed that a variation in the osmotic pressure of the external medium equal to a depression of freezing point of 1 . 7 O C brings about changes of 0.3"C and 0~6°Crespectively in the osmotic pressure of the blood. The intracellular osmotic pressure is adjusted to the osmotic pressure of the blood in part by changes in water content of the muscles and (4) by the variation in concentration of a number of intracellular amino acids, namely glutamine, glycine, proline and alanine, but, not taurine. Taurine is present in considerable quantity but, in the case of Palaemon, whereas there is an 85% decrease in amino acids on transference t o 30% sea water, the taurine level only falls by 70/-10%. Similarly in Carcinus, in which the osmotic pressure of the blood is maintained above that of the surrounding medium when the latter is diluted, the osmotic pressure of the muscle fibres changes proportionately with the blood (Shaw, 1958b). The reduction in the osmotic pressure of the muscle fibre is brought about, in part at least, by the loss of the non-ion fraction composed of free amino acids, taurine, betaine and trimethylamine oxide. These account for about two thirds of the total osmotic activity. The regulation of these substances is therefore quite different from that of the inorganic muscle ions, the concentration of which, in earlier work (Shaw, 1955, 1958a) had been shown to be governed solely by the dilution of the muscle contents by the osmotic intake of water following the dilution of the blood. The experiments on Carcinus showed that the regulation of intracellular organic nitrogenous substances was completely reversible, the normal muscle concentrations being regained when thc animal was replaced in full salinity seawater. He suggested two possibilities which might explain this regulation. Either the substances are removed from the muscle fibrc during blood dilution, or they are combined with other muscle constituents, thus losing their activity. The concentration of these substances in the blood is always low, which might suggest that if they are not temporarily removed from the fibre, they combine with large molccules within the cell, and are thus rendered osmotically inactive, but this has yet to be confirmed (see p. 238). Analysis of other crustaceans, which are purely marine and do not adapt to brackish water (e.g. Homarus and Nephrops) has shown that in these

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species organic nitrogenous substances are present in much the same concentration as in Carcinus (Shaw, 1958b). It seems likely that Carcinus utilizes a situation which already exists. The reason for the presence of organic nitrogenous compounds is possibly morc obscure than a t first sight. The ionic composition of the muscles of marine animals is fairly similar t o that found in many terrestrial and frcshwatcr animals, and it may be that there is an optimum ionic conccntration for striated muscle fibre. I n marine animals therefore, thc high osmolar concentration is made up by the addition of organic nitrogen compounds and the development of the ability t o regulate these compounds makes it possible for a marine animal that is unable t o osmoregulate its internal environment (e.g. Arenicola) t o penetrate into brackish watcr. I n animals like Carcinus which osmoregulate the blood, the two processes possibly supplement each other (Shaw, 1958b). The remarkable efficiency of the regulation in Carcinus was shown by Duchiiteau et al. (1959) studying the response t o the change in osmotic pressure produced by moulting. At emergence the blood osmotic pressure is suddenly decreased, yet the decrease of intracellular amino acids in response t o this is sufficiently rapid t o prevent any hydration of the muscles. They too conclude that this regulation must be t o maintain the inorganic composition of the cells in the presence of changcs in the osmotic pressure of the surrounding fluid. Shaw (1959) studied the effects of changing the salinity of the surrounding medium of an animal which would not be expected t o possess this intracellular osmotic regulation. He adapted the freshwater crab Potamon niloticus (Milne-Edwards) t o different concentrations of sca water and found that up t o 50% salinity there was not as much dehydration of the muscles as would be expected by simple osmosis. This implies some small addition of osmotically active substances t o the muscle and in fact there is a slight increase in intracellular amino acid concentration up t o 75% salinity. Above this salinity, however, no more amino acid is added. Osmotic regulation of the internal medium has been shown t o occur in Astacus (Duchiiteau and Florkin, 1961), Nereis (Jeuniaux et al., 1961a), Leader (Jeuniaux et al., 1961b) and Eriocheir (BricteaxGrBgoire et al., 1962) and complete poikilosmosity, i.e., no regulation of the internal medium, in Arenicola (Duchiiteau et al., 1961), Perinereis (Jeuniaux et al., 1961a), Mytilus (Bricteax-GrBgoire et al., 1964a) and Gryphuea (Bricteax-GrBgoire et al., 1964b). I n all these animals aminoacid concentration increases with increasing salinity, the increase bcing greater than would be accounted for by changes in hydration. The amino acids which show the greatest changes in concentration are alanine, glycine, glutamine and glutamic acid, proline and arginine,

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the importance of each varying in different species. Taurine was not determined in these earlier analyses, but Jeuniaux et al. (1961b) found taurine in considerable quantities in Leander ; however, in this species it shows little change with changing salinity but, when Eriocheir is transferred from fresh water t o sea water there is a rise in the taurine level. The first demonstration of taurine playing an important role in intracellular osmotic regulation in an animal was in Asterias rubens Linnd (Jeuniaux et al., 1962a and b). They found that when Asferias, that had previousIy been living in full salinity, were introduced into water of 60% salinity they first became very bloated, but that after 48 h they became less bloated and resumed normal activity and survived in the brackish water for a t least ten days. During their adaptation t o dilute sea water the osmotic pressure of the perivisceral fluid is the same as that of the external medium; however, the tissues of the gastric caeca showed only a slight increase in hydration (72% of fresh weight in experimental animals as compared with 68% of those in full sea water). At the same time, the concentration of free amino acids and taurine had decreased from 22-1 m moles/100 g fresh tissue t o 12-2 m moles/100 g fresh tissue-which is equivalent t o a depression of freezing point of 0*28OC, while the dilution of the intracellular contents only accounts for the equivalent of 0-04"C. The change in the intracellular concentration of the amino acids is almost exclusively due t o the loss of glycine and taurine (1300-710 mg/100 g fresh tissue and 490280 mg/100 g fresh tissue respectively). Similar studies on intracellular isosmotic regulation in Mytilus, Gryphaea and Ostrea show the importance of taurine and also glycine, glycine-betaine and alanine (Brideax-Gr6goire, 1964a and b). Thus when Mytilus edulis is adapted t o water of half salinity, the isosmotic intracellular regulation is accomplished by a slight change in hydration and above all by a decrease in concentration of sodium and chloride ions and amino acids of which taurine accounts for approximately 10%. Taurine appears t o have a special relevance in the isosmotic regulation of euryhaline bivalves. Thus, Lange (1963) measured total ninhydrin positive substances (i.e., amino acids and taurine), and taurine separately in Mgtilus and found that both were linearly correlated with salinity, but, in addition, taurine formed an increasing percentage of the total with decreasing salinity (Fig. 2). Lange (1963) points out that taurine in iMytilus exerts a " sparing effect " on the use of amino acids in the osmotic equilibration of the cells. Florkin (1963) had already suggested that all major organic solutes of the cells are non-essential t o the animals.

237

TAURINE IN MARINE INVERTEBRATES '5

200 -

i0

150

i

-

i .-uC

L

100 -

a

2

a In .

z5

Z 50

-

o-x

/ lb

I

20

I

30

0

FIQ.2. The correlation between sea water salinity and the concentrations of NPS and taurine, respectively. NPS (ninhydrin positive substances), determined as taurine equivalents; x - x taurine. Redrawn, from Lange 1963.

Florkin (1962), Florkin et al. (1964) and Florkin and Schoffeniels (1965, 1969) in studies on the adaptation of Eriocheir from sea water to fresh water measured nitrogen excretion and the amino acid content of muscle tissues. They found that the decrease in intracellular amino acid concentration in Eriocheir adapting t o fresh water is accompanied by a transitory increase in nitrogen excretion, mainly in the form of ammonia. After the first two days of adaptation t o the new environment, nitrogen excretion returns t o the initial value. Conversely, when Eriocheir is adapted t o sea water from fresh water there is a pronounced decrease in excreted nitrogen. The former could be indicative of an increased rate of amino acid degradation, while the latter could be due to a decrease in the intensity of the degradation process, or an increase in amino acid synthesis. Shew (1958a and b) from earlier work on Carcinus suggested that the increase in free amino acid content of the muscle is derived from a protein reserve and vice versa. However, Florkin et al. (1964) found that the proportion of alanine, proline and leucine present in the muscle as free form as opposed t o that. found in

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protein did not alter with adaptation suggesting that the latter hypothesis is unlikely. Schoffeniels (1964) also rejects this possibility and claims that any total number of moles of amino acids in a cell depends on a balance between synthesis and breakdown of these substances in the cell. He postulates that the rate of amino acid production, as well as the rates of transamination and dehydrogenation are directly dependent on the ionic composition of the cell. The sea urchin Strongylocentrotus droebmhiensis (Mueller) exhibits isosmotic intracellular regulation (Lange, 1964) but it is less efficient than euryhaline invertebrates. The increased length of time needed t o adapt to new salinity conditions allowed Lange (1964) to study the stages of isosmotic intracellular regulation. He found that this is in response to increased cellular volume. Thus when an animal is placed in dilute sea water the cells take up water by osmosis. The animal remains swollen for a week and on the eighth day it returns t o its normal size. The cause may be a change in permeability of the cell membrane to amino acids and taurine which allows these substances to be excreted together with inorganic ions and water or, there may be a change in the equilibrium between amino acids and, for example, protein which has the effect of removing some of the osmotically active substances thus causing the osmotic excretion of water. Lange (1964) does not consider this latter explanation likely because taurine, which he regards as an excretory product, would not go into a combination in the cell. The change is probably a transitory process, since sea urchins living in dilute sea water still contain high concentrations of intracellular amino acids. The original properties of the cell membranes must be restored once the cell volume is regulated. Lange (1964) regards the correlation between salinity and the concentration of intracellular amino acids which " enables the animal to keep their intracellular salinity on a level compatable with life " as being an expression of one of the processes which makes the regulation of cell volume possible. But, the presence of large quantities of taurine in stenohaline species might suggest that it is present as a matter of course, and is simply utilized by some animals as a regulatory substance. Although never suggested for marine invertebrates, the considerable quantities of taurine present in muscle may play a part in energy release (Bascheri and Fromageot, 1962). Taurine appears to have a facilitating effect on the action of insulin on extracellular glucose in mammals (Macallum and Sivertz, 1942 ; Donadio and Fromageot, 1964). The function of isethionic acid in ion balance of nerve cells has already been mentioned (p. 230). Taurine itself also appears t o play a part in nerve function. It is a structural analogue of y-aminobutyric

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acid (GABA), a specific inhibitor of impulse transmission in the central nervous system. Taurine, too, inhibits transmission of nerve impulse both in mammals (Curtis and Watkins, 1961) and in marine invertebrates (Dude1 et al., 1963; Kravitz et al., 1963a and b). The inhibitory effect is much smaller than in the case of GABA (Kravitz et al., 1963b ; Edwards and Kuffler, 1959). Similarly L-cysteic acid and L-cysteine sulphinic acid, precursors of taurine, like glutamic acid, the precursor of GABA, have an excitatory effect on impulse transmission, but the content of taurine in motor and inhibitor axons is the same (Kravitz et al., 1963a). Recent work on marine algae does provide a hint of a further possible function of taurine in marine invertebrates and molluscs in particular. Taurine is mainly found in those marine algae which contain relatively large amounts of polysaccharide sulphates (Schweiger, 1967). This had previously been noted by Lindberg (1955)and both these authors take the view that the polysaccharide sulphates may be formed from taurine via a transesterification reaction involving choline sulphate. The same argument may be applied to marine bivalves and gastropods, many functions of which depend on a copious supply of sulphonated polysaccharides. The Mollusca, more than any other phylum, are noted for their high taurine content (see p. 211). Simpson et al. (1969)suggested the possibility that taurine is not produced by invertebrates but acquired from their diet. While it is undoubtedly true that marine invertebrates are capable of forming taurine-these authors were sceptical even of this, reasoning from the wide range of values in animals from the same environment-taurine may well be obtained from their diet. Thus taurine is known to be present in a wide range of algae (Table 111). It is present in only trace quantities in sea water even though it is known to be excreted unchanged by animals (Webb and Johannes, 1966, 1967). However, marine bivalves, e.g., Mya and Tellina, can take up taurine out of solution (Allen, personal observations). It is questionable whether quantities of taurine present in food play anything more than a minor role in providing taurine. However, cysteinolic acid present in Ulva and Enteromorpha (Ito, 1963) and Polysiphonia (Wickberg, 1957) has been reported in the gastropod Siphonaria zelandica, which has also a rich taurine content (Bedford, 1969). A pathway from D-cysteinolic ucid (2-~-amino-3-hydroxyl-l-propane sulphonic acid) to taurine, while likely, has yet t o be reported. Little work has been carried out to indicate the significance of the different quantitiesof taurinepresent indifferent animalsof the same class, for example, in the Annelida and in the Mollusca. Stevens et al. (1961)

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did suggest that the lower levels in Limulus as compared with Cancer and Homarus is but a reflection of its evolutionary history and development. Only Hillman (1964, 1966) has compared the taurine content of populations of the same species, in this case Crassostreu virginica (Gmelin). He compared the taurine levels in addudor muscles of specimens from three populations from different salinity regimes, which he kept in varying experimental salinities. Thus specimens from high salinity environment (28%,) always had a higher taurine content than those from a low (lo%,) irrespective of the experimental salinity in which they were both kept. However, those from intermediate environmental salinities, and which showed intermediate values at high experimental salinities, a t an experimental salinity of 12%, had a taurine concentration equal to that of the population from the high salinity environment under similar experimental conditions. Apart from deducing an osmoregulatory role Hillman ( 1966) considered these differences t o be physiological manifestations of genetic differences among allopatric populations which have adapted their osmoregulatory mechanisms t o various salinity regimes. AND CONCLUSIONS IV. SUMMARY Taurine is not only an oxidative end product but also a key intermediate of sulphur metabolism. I n marine invertebrates it appears to have three organic functions. The best documented is its function in intracellular isosmotic regulation where it (and " non-essential ')aminoacids) are preferentially lost when the salt concentration outside the cell is lowered (p. 233 et seq.). It should be pointed out that at all times the taurine concentration is low in the haemolymph (e.g., Kermack et al., 1955; Allen, personal observations). It can be shown that specimens of Mya subjected t o low salinities greatly increase the rate of loss of ammonia from their bodies (Allen and Garrett, 1971). However, no comparable increase occurs in excreted sulphate ions, which might be expected from the degradation of taurine, nor in taurine itself. Thus, it could be that sulphate ions are retained in the body or possibly might be attached t o mucopolysaccharides and disposed of by enhanced mucus secretion. The other known functions are concerned with transphosphorylation, this particularly in marine polychaetes (p. 225), and with the rate of transmission of nerve impulses (p. 230) and the ionic balance of nerve axoplasm. In connection with the latter function it should be pointed out that the ventral nerve cord of the lobster can fix C1402and that labelling occurs in taurine and in aspartic and glutamic acids (Schoffeniels, 1968 ; Florkin and Schoffeniels, 1969). Experiments using glucose-U-14Cindicates that in the case of rtlanine, serine and glycine

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the hydrocarbon skeleton is derived from pyruvate or an intermediary of the Krebs cycle. Taurine also had a specific activity similar to alanine and together with aspartic acid, proline and glycine makes up most of the concentration of amino derivatives present (0.5-2 p moles/ 100 mg fresh weight). I n similar experiments using D-arabinose U14C, activity in taurine, aspartic and glutamic acids demonstrates that the L-ketoglutaride may be produced outside the operation of the Krebs cycle and would indicate that a metabolite of this sequence is common t o both taurine and 2-ketoglutarate (Florkin and Schoffeniels, 1969). In fact, the pathway picture is complex (Fig. 1) but out of a variety of possible routes from cysteine that via cysteine sulphinic acid and hypotaurine and that via cysteamine and hypotaurine seem to be the most significant in marine invertebrates. Clearly a vast amount of experiment is necessary t o elucidate the chemistry and function of taurine, but we believe sufficient is now known t o emphasize that this is a compound of considerable significance in the physiology of marine invertebrates.

V. ACKNOWLEDGEMENTS We would like t o thank Miss Audrey Twizell for her patience and good humour in coping with our demands for typing what at times was barely decipherable notes t o finished manuscript, and also Miss Carol Miller for assistance with the references. Not least we wish t o thank Professor Arthur Martin of the Zoology Department, University of Washington, Seattle, who so carefully read the manuscript and who made many valuable comments. VI. REFERENCES Abbott, W. and Awapara, J. (1960). Sulfur metabolism in the the lugworm, Arenieola crbtalcr Stimpson. Biol. Bull. mar. biol. Lab., Wood8 Hole, 119, 357-370. Ackcrmann, D. (1935). Asterubin, eine schwefclhaltige Guanidinverbindung der belcbtcn Natur. Hoppe-Seyler’a 2.phyawl. Chem. 232, 206-21 2. Ackermann, D. (1930). ubcr das Verhaltcn des Taurocyamins im Stoffercchscl und das Vorkommen von Glycocyamin im Ham. Hoppe-Seyler’a 2.phyaiol. Chem. 239, 231-235. Ackcrmnnn, D. (1955). ubor das Vorkommcn von Homarin, Taurocyamin, Cholin, Lysin und andcren Aminosauren sowic Bernstoinesaurc in dem Mccreswurm Areiticola marina. Hoppe-Seyler’a 2.phyeiol. Chem. 302, 8@86. Ackermann, D. and Janka, R. (1954a). Neues Vorkommcn von Mytilit bei Avcrtcbraten (Ciona inteetinalb). Hoppe-Seyler’a 2. phyaiol. Chem. 296, 283-286. Ackcrmann, D. and Janka, R. (195413). uber das Verkommen von Homarin, Glykokollbctain, Cholin, Argenin, Mytilit, Taurin and d, 1-Milchsiiurc in der Moercsschnecko Patella apuriens. Hoppe-Seyler’a 2. phyaiol. Chem. 298, 65-69.

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UPWELL NG AND THE PRODUCTION OF FISH D. H. CUSHING Fisheries Laboratory, Lowestoft, England

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I. Introduction 11. The Physical Background 111. The Biological Background A. The Production Cycle in an Upwelling Area B. The Part played by Nutrients in an Upwelling System . IV. Description of 8 Well-known Upwelling Area A. The California Current System B. The System in the Gulf of Panama .. The Upwelling area^ .. V. A. The Width of the Upwelling Zone . .. B. Upwelling Areas in the Eastern Boundary Currents C. The Indian Ocean D. The Equatoriel System .. E. Domes end the Eastern Boundary Currents F. Minor Upwellings . VI. The Production of Living Meterial in the Upwelling Areas A. Primary Production . B. The Production of Zooplenkton C. The Production at the Third Trophic Level D. The Transfer Coefficients VII. The Biology of an Upwelling Area VIII. Discussion .. .. IX. References

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I. INTRODUCTION In the history of oceanography, the study of upwelling is comparatively recent. Nathansohn (1906) had suggested that a local vertical movement in Mediterranean waters generated higher production. But it was not until the results of the " Meteor " expedition were published during the thirties that the physical and biological significance of upwelling was realized. Schott (1902), with the aid of vertical sections across the continental shelf from north of the equator to the Cape of Good Hope, described the physical mechanism of upwelling in the Benguela current. From the " Meteor " material, Hentschel and Wattenberg (1930) associated areas of rich production all over the equatorial and southern Atlantic with nutrients which had risen from below. Upwelling had been described physically before, for example by 255

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McEwen (1929) off California, but the scale of the phcnomcnon was first described thoroughly on the " Meteor expedition. The biologists did not explore the upwelling arcas to any great extent until quite recently. Gunther's (1936) exploration of the Peru current was the first explicit examination, followed by Steemann Nielsen's world survey in the " Galathea )' expedition. A fortunate outcome of this apparent disinterest is that when the upwelling areas were explored they were examined with standard equipment, the radiocarbon method of measuring primary production and the 1 m plankton net, or its variants. Since the early fifties many expeditions have sailed, covering much of the Pacific and Indian Oceans and some continuing work has been executed in the Atlantic ocean. Most of the expeditions were designed to study large-scale physical phenomena and at the stations they occupied, biological observations were also made. The work off California was aimed at a more specific objective, to discover why recruitment to the Californian sardine fishery had failed. An expedition to the Benguela current was carried out by the '' Discovery ') Investigations/NIO to explore the production there. It would be churlish for a biologist to describe the Indian Ocean expedition as one designed to extract physical information only, because much biological information of great interest emerged, but perhaps a fuller study of upwelling in the Bay of Bengal and upon the Malabar coast of India can now be carried out. The present study was made for F A 0 as part of its IWP project (Indicative World Plan). The aim was to make a projection of world fish production during the decade 1975-85. As the upwelling areas comprise the most promising ones for exploitation in tropical and subtropical waters, an attempt was made to estirnatc possible production from estimates of primary and secondary production. Some areas, such as that off Peru, arc already well exploited but others, such as that off Southern Arabia, are not. We may distinguish three forms of production in tropical and subtropical seas, the coastal upwellings (within 100 km of the shore), the offshore divergences round the edges of the subtropical anticyclones, and the central areas. Here thc first two have been examined but not the third. This is because the present fisheries depend primarily upon herring-like and cod-like fishes. To exploit the whole ocean (in addition to the tuna), the small fishes of the Deep Scattering Layer, e.g. myctophids, should be caught; they can be caught, but because they are dispersed they cost too much to exploit at the moment. The conclusion to this work is that the catches available in the upwelling areas amount to about 100 million tons, a fair proportion of ')

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which is already being taken. Nearly 10 million tons are taken from the Peru current and there are catches being made now in nearly all of the areas. Therefore there is a limit to the expansion of the present world catches (of 60 million tons). Further, the possibility of feeding the expanding world population from conventional fisheries is distinctly limited, if only because most of the present catch is taken by the developed countries, as fish meal or as frozen fish. In the deep ocean, the tuna or fourth level is already well exploited, which leaves the tertiary level such as myctophids ; there are large quantities of these, but rz new technology is needed to exploit them. There are three by-products of the investigation. Tho first is a rough model of production in upwelling water which suggests that, if upwelling is too fast, the production becomes vulnerable to grazing too early in the cycle and so the total production in a time period is less than it might have been. The second by-product is an analysis of the relation between phosphorus in the water and production ;it is suggested that the well-known correlation between phosphorus and zooplankton occurs because the quantity of nutrients in the sea may depend upon production and not the other way round, as has been so often suggested. The third by-product is a comparison of transfer coefficients from primary to secondary production, which suggests that the coefficient decreases with increasing primary production.

11. THE PHYSICAL BACKGROUND In each of the three major oceans, the largest structures are the two subtropical anticyclones, one north and one south of the equator. In each, the western boundary current (for example, the Kuroshio, the Gulf Stream and the Somali Current in the northern hemisphere) is swift and narrow (up to 4 knots in the northern hemisphere) and the eastern boundary current is broad and slow (about 4 knot) and tends to be somewhat reduced in salinity because it originates in rainy areas. In the Pacific, the eastern boundary currents are the California Current and the Peru Current and they are linked to the equatorial currents directly and also by the California Extension and the Peru Oceanic Current. I n the Atlantic, the analogous currents are the Canary Current and the Benguela ;in the Indian Ocean, the monsoons dominate the upwelling structures, but there are minor eastern boundary currents on the Malabar coast of India, off the Andaman Islands and off N.W. Australia. There is upwelling in the eastern boundaries because the winds tend to blow parallel to the coast towards the equator (Wooster and Reid, 1963) ; in summer time, the high pressure systems lie very roughly above the subtropical anticyclones and so the winds, which,

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nearer the equator turn into the north-east and south-east trades, must blow along the coast, northerly in the northern hemisphere and southerly in the southern hemisphere. As the wind blows parallel to the coast towards the equator, the water is moved offshore by Coriolis force and, because the movement does not extend far in depth, water is drawn from below near the coast. As the water is blown offshore at an angle to the coast it is moved towards the equator. At about 100 km offshore there is often a convergence where the water sinks and, a little further offshore, a divergence, generating a secondary source of upwelling above the thermocline (Hart and Currie, 1960). Sverdrup (1938) called this region the dynamic boundary; in this area, the flow towards the equator is intensified and Sverdrup (1938) called it a convection current. There are often large swirls in fixed positions, between local upwelling systems (Reid et al., 1958). The current flowing towards the equator at the surface is compensated by a countercurrent below about 200 m flowing towards the pole (Gunther, 1936; Reid et al., 1958; Hart and Cunie, 1960). Further, there may be narrow surface countercurrents generated inshore during the period of upwelling (Reid et al., 1958; Wyrtki, 1963). The depth of the whole upwelling system is shallow, less than 200 m, and its offshore boundary is imprecise. Wooster and Reid (1963) make the generalization that upwelling is found in the eastern boundary currents of the subtropical anticyclone. Upwelling could occur in the western boundary currents because the wind blows parallel to the coast and Coriolis force would carry the water offshore, if the existing currents were not so swift and stable ; in other words, the forces generating upwelling are local and weak, whereas those generating the western boundary currents are strong and spread across the whole ocean. The Somali Current in the Arabian Sea is a special case because it tilts when it swings eastwards t o the south of Socotra Island (Warren et al., 1966) and cool water upwells on the coast south of Cape Gardafui, the Horn of Africa. It is interesting that off the Malabar coast an upwelling is generated at the end of the south-west monsoon as the current tilts (Darbyshire, 1967). In higher latitudes, the circulation tends to be cyclonic (for example in the Alaska gyral) and when the wind blows parallel to the coast and towards the pole on western coasts, the water is moved towards the coast by Coriolis force and so there is a tendency for the water to sink. On eastern coasts, under such conditions, upwelling can occur, as happened off Nova Scotia in September during a period of south-westerly winds (Hachey, 1936-37). When the wind blows parallel to the coast and towards the cquator on eastern coasts there should be sinking, as Longard and Banks

IJPWELLINO AND THE PRODUCTION OF FISH

259

(1952) showed off Nova Scotia. But there are biological reasons why upwelling is only noticeable, in biological terms, in tropical and subtropical seas as will be explained below ; in the cool water, rising from below, a quasi-temperate production cycle is generated, which is in sharp contrast (in its high production) to the steady state system of tropical waters. Kilometres

0

0

0

o o

Surface drift towards the Countercurrent

towords

equotor

the pole

FIQ.1. A diagrammatic vertical section of an upwelling area. The full line represents tho upwolling and offshore drift to and beyond the dynamic boundary. or " roller bearing " at 100 km from the shore. Because the upwelling system drifts towards the equator, the upwelled water moves outwards at a slight angle to the coast.

Figure 1 is a diagram of an ideal vertical section through an upwelling area (adapted from Sverdrup, 1938; Hart and Currie, 1960; Bang, 1071). Above 200 m the water moves towards the equator and the upwelling system lies within this zone ; below it the countercurrent moves towards the pole. The coastal upwelling is bounded between 50-100 km offshore by the cell of convergence and divergence, the region at which Sverdrup (1938) put his dynamic boundary. Inshore of this boundary there is a region of slow mixing of old and new upwelled waters, and offshore of it there is a region of divergence, a secondary form of upwelling. The cell of convergence and divergence,

260

D. H. CUSHINU

or “ roller bearing ” as Hart and Currie (1960) called it, is also an agent of offshore transport. The secondary upwelling offshore of this boundary is generated by the vorticity of the wind stress. The divergences in the equatorial currents and elsewhere are created by the same agency (Hidaka, 1958). There tend to be divergences along the poleward boundary of the subtropical anticyclones at the western ends of the equatorial currents and along the equatorial boundary of the southern anticyclones ; similarly there are convergences along the eastern equatorial currents, particularly in summer along the equatorial boundary of the northern anticyclone (Hidaka and Ogawa, 1958). But there are also upwelling areas where the equatorial currents are formed ; the Costa Rica Dome is the most well known, at the root of the North Equatorial Current in the North Pacific, but there are analogous phenomena in the East Atlantic and East Indian Oceans. Recently, Smith (1969) has described the development of the theory of upwelling. Sverdrup (1938) and Sverdrup and Fleming (1941) examined upwelling in terms of Ekman’s theory of transport ; from the change in the distribution of properties, during a short time, it was shown that the surface water was carried away from the coast of California to be replaced by water from below. Hidaka (1954) and Yoshida (1955, 1967) developed steady state, transient state and quasi steady state models. From Yoshida’s theories, it was suggested that the coastal upwelling zone was about 50 km wide in middle latitudes, which was observed by Smith et al. (1966) off Oregon, U.S.A. His theory further suggests that the width of upwelling decreases with latitude, which explains the extensive areas of upwelling and of the production of living material in all three eastern tropical oceans; further, the countercurrent flowing polewards in a major upwelling system is homologous with the equatorial countercurrent. An interesting consequence of Yoshida’s theory is that coastal processes respond more quickly t o winds which vary in time than the steady ones. Arthur (1965) has examined the role of vorticity in upwelling and reaches much the same point as Yoshida: in addition, he showed that upwelling is more intense on the equatorial sides of capes. One of Smith’s important conclusions is that there is quantitative agreement between theory and observation ; his paper should be consulted for a good introduction to the physical theory of upwelling. Figure 2 is a diagram of the upwelling systems in an ideal ocean, based on observations in the Pacific, showing the coastal upwellings in the eastern boundary currents, the divergences and convergences in the equatorial current system and the eastern dome. Also shown are the divergences on the-poleward boundaries and offshore of the coastal

261

UPWELLING AND THE PRODUCTION OF FISH

Eastern boundary upwelling area

I_

Divergence

1

Convergence

Dome

NEC North Equatorial Current Current SEC South Equatorial Current SECC South Equatorial Countercurrent ECC Equatorial Countercurrent EUC Equatorial Undercurrent FIQ.2. Diagram of the distribution of upwollings and divergences in the anticyclones of an ocean. , *

upwellings (based on Hidaka and Ogawa, 1958). Between the Equatorial Countercurrent and the North Equatorial Current there is a zone of convergence (Cromwell, 1958; Hidaka and Ogawa, 1958; Wyrtki, 1966). The system is not centred precisely on the equator, but is offset somewhat to the north, so that the Equatorial Countercurrent occurs between 5 and 10"N and the northern edge of the South Equatorial Current lies about 3"N. At about the equator, the north and south equatorial gyres meet, forming a westbound North Equatorial Current (at 10-20'N in the Pacific) and westbound South Equatorial Current (at 3"N to 10's in

262

D. H. CIJSHINQ

the Pacific). Between the two equatorial currents runs an eastbound Equatorial Countercurrent (at 5-10°N in the Pacific). At the equator beneath the South Equatorial Current runs the eastbound undercurrent, or in the Pacific, the Cromwell Current, which runs between 140OW and the Galapagos Islands. I n the western ocean two undercurrents may appear beneath the North and South Equatorial Currents. Figure 3 shows how the currents are resolved in the eastern tropical Pacific and it is clear how much Fig. 2 depends on this diagram (Wyrtki,

2 0"

2 0" 14 0"

120"

100"

80'

FIG.3. Currents in the eastern tropical Pacific during the period June to December (Wyrtki, 1966) ; the figures represent transports in cm3. I012/sec.

1966); notable is the great width of the system. There is an area of offshore divergence spreading from the upwelling areas to the equatorial currents which corresponds t o the broad area of upwelling in low latitudes postulated by Yoshida (1967). I n the equatorial complex shown in Fig. 3, the two equatorial currents tend to generate divergences and the countercurrent, convergences. Beneath the Cromwell Undercurrent, at the equator, radiolarian skeletons are deposited in relatively dense quantities (Arrhenius, 1963). There is a productive zone, narrowly confined to the region of the undercurrent, which is more productive than the divergences of the South

263

UPWELLING AND THE PRODUCTION OF FISH

Equatorial Current near the equator. The same point is made in Fig. 13 (p. 295) showing the distribution of radiocarbon observations, u iiarrow productive band at the equator in the eastern ocean above the Cromwell Undercurrent. The seasonal variation of the equatorinl systcm has been described in the Pacific by Knauss (1963) and Table I summarizes his findings. TABLEI Seuaon

September to J a n u a r y February to April May to J u l y July, August

North Equdorial Cuwent

Countercuwent

Weak Strong Strong Weak

Weak None Strong Strong

SOUllb Equalorid Current Strong Weak Weak Strong (ICnauss, 1963)

Figure 4 is a diagram of the seasonal cycle of upwelling in an eastern boundary current and in the equatorial system. It is based partly on Wooster and Reid's (1963) estimates of Ekman transport normal to the

\

\-

4' 0

tt Winter

Spring

I

I

I

I

I

1

V

l

l

l

Summer

Autumn

Coastal upwelling

1Divergence

Current

I

2 Convergence

Extensive area of divergence

Fro. 4. Diagram of the seasonal cycle of upwelling in a n eastern boundary current and of divergence in an equatorial current, based very roughly on tho system in North Pacific anticyclone.

264

D. H. CUSHINO

coast. It shows the movement towards the pole of thc coastal upwelling systems from spring to autumn as the subtropical high intensifies, and the strengthening of divergence along the Equatorial Current in winter and spring. The diagram does not show that events in the southern hemisphere are bigger and more persistent, which they are. This may be because stronger winds originate in the Southern Ocean, or because the coastlines have the best shape for the seasonal distribution of the direction of the trade winds. The distribution of divergences and convergences is taken from Hidaka and Ogawa’s (1958) charts. There are wind-driven upwellings and geostrophic upwellings, both in coaatal areas and in oceanic areas. Coastal upwelling is generated by winds blowing parallel to the shore towards the equator, as in the major upwellings, or is generated geostrophically by the tilt of a current, as in the Somali Current (Stommel and Wooster, 1965). Some areas may include both wind-generated upwellings and geostrophic upwellings, as for example, off the Malabar coast (Darbyshire, 1967). There is a. specialized form of upwelling off Cabo Frio in Brazil where warm salty water offshore sinks and is replaced inshore by cooler less salty water and this process is assisted by north-east winds (Emilsson, 1961). Oceanic upwelling includes both the divergences due to the vorticity of the wind stress, all around the subtropical anticyclones, and the geostrophic upwellings within the equatorial system itself, as for example above the undercurrent and in the domes.

111. THE BIOLOGICAL BACKGROUND

A. The production cycle in an upwelling area In temperate waters, the pattern of production cycles is dominated by seasonal changes. During the winter, production cannot take place when the depth of mixing is greater than the critical depth, at which production equals respiration, both integrated from the surface (Sverdrup, 1953). Production starts when the critical depth becomes greater than the depth of mixing. The depth at which the rate of production equals the rate of respiration is called the compensation depth. After production starts, its rate of development is governed by the ratio of compensation depth to depth of mixing (Cushing, 1962). So the rate at which production develops in the temperate spring is determined by the amount of sunlight and the strength of the winds, and other factors causing mixing, all of which vary seasonally. The production cycle in an upwelling area resembles that in temperate waters. The cool water which originates from depths of less than

UPWELLINQ AND THE PRODUCTION OF FISH

265

200 m contains a resident and sparse population of plants and animals,

very like those in temperate waters in early spring. At the bottom of the photic layer, the algae start to divide and, as in temperate waters, the increase in animal production is caused by the increase in plant population because the reproduction of the animals depends upon this increased food ; hence the animal production follows the plant production in time. Thc lag between plants and animals may be as much as half a generation and it allows the production of large stocks of plants, and, later, of animals as in temperate waters. In contrast, in the deep subtropical ocean, there is no sudden increase in the production rate of the plants, and there is no delay between plant and animal production and there are low stocks (Cushing, 1959). If the production cycle in an upwelling area were similar to that in temperate waters, a bell-shaped curve of production would be expected as a function of distance from the point of upwelling, similar to the temperate curve as a function of time. The photic layer is usually fairly deep, up to 50 m, and the rate of upwelling is rather slow, of the order of 1 m/day (McEwen, 1929; Hidaka, 1954; Yoshida, 1955). So production must rise slowly from the bottom of the photic layer, taking many days to reach the surface. I n the first days of the process, from the 1% light level to the 5% light level, the increase in production is necessarily very slow, but it must increase exponentially as upwelling proceeds. Because the depth of the photic layer is many times the daily upwelling distance, the peak production is probably reached near the surface not far from the point of upwelling (the problem is set out formally in a later section). On reaching the surface, the plant and animal populations must move away from the point or line of upwelling and because the rate of upwelling is a very small proportion of the speed of the eastern boundary currents, such movement must be at an angle to the coast. The production along this line of movement is high and appears to decrease slowIy with distance, and the band of maximum production appears to be rather wide and to decrease rather slowly with distance from the coast. If the production cycle were symmetrical in time, it would continue for about the same time = the water takes to rise in the upwelling process. At 4 knot, an upwelling which took 30-60 days to rise through the photic zone might drift 300-600 miles before the decay process was complete. This is a simplified view of the process. Because of mixture and additional divergence offshore, any neat vector of production does not exist. But the broad band of production declining rather slowly from the coast is the result of the upwelling production cycle and the additional processes.

266

D. H. CUSHINO

The dynamic boundary at about 100 km from the shore marks the edge of the coastal upwelling, as noted in the previous section. But divergences continue to seaward and the biological boundary must be at the imprecise edge of the wind system. The boundary in zooplankton (Thrailkill, 1956, 1957, 1959, 1961, 1963) or surface phosphate-phosphorus (California,Department of Fish and Game, 1958) is often beyond the dynamic boundary, perhaps hundreds of kilometres. As a convention, the biological limit of the upwelling area is taken as half the maximum from the coast. Zooplankton quantity is used as a convenient index of summed production over a period and phosphate-phosphorus is used because it correlates so well with the zooplankton; this remarkable correlation is discussed in detail in the following section. Some evidence will be put forward below to show that the width of the zone of biological production as defined above is about two and a half times the distance to the dynamic boundary. The production cycle in the upwelling areas is noticeable because it is really a discontinuous temperate cycle of high amplitude which is contrasted with a continuous sub-tropical cycle of low amplitude in the deep ocean well offshore of the upwelling area. Then it is not accidental that the whole community structure as shown in the California current is really a temperate one as will be shown below. The plankton communities are much less diverse than those of the deep tropical ocean ; the bathypelagic fishes of the deep ocean are not very abundant in the upwelling zones proper, but like the tunas they are found outside the dynamic boundary 100 km off the coast. Thus, an upwelling area outside the subtropical anticyclones may be of relatively little importance because the effect of upwelling cannot be distinguished from the ordinary temperate cycle of production. In the Antarctic there is a slow and extensive high amplitude pulse of production which is correlated with the seasonal changes of light intensity ; the existence of deep upwelling at all seasons against the shelf is an unnecessary source of explanation. Thus, for physical and biologicd reasons, the study of upwelling is effectively limited to the subtropical anticyclones. The cycle of produchion in an upwelling area is considered as a temperate cycle rising slowly from the bottom of a fairly deep photic layer. Because of a slow and continuous mixture, with a steady addition of living material at the coast and offshore, the distribution of biomass in an upwelling area is fairly uniform. Because divergences continue far offshore beyond the dynamic boundary at 100 km, the width of the upwelling area, biologically, is considered to extend beyond the obvious physical boundaries.

WWPkLIlk2 d D "HE PRODUCTION OF FtbE

967

B. The part played by nutrients in an upwelling syslent The high production in thc subtropical upwelling arcas and in the Antarctic is often attributed to the associated presence of high nutrients which have reached the surface from below in the upwelled water (Hentschel and Wattenberg, 1930 ;Deacon, 1937). As nutrients become reduced, the algal reproductive rate may decline; Riley (1946), on the basis of an experiment by Ketchum (1939), suggested a level of 0.55 pg atoms PO,.P/l. below which the algal reproductive rate becomes reduced. Ketchum's experiment showed that the quantity of algae produced was proportional to the quantity of phosphorus available. A repetition of this experiment confirmed this result, but showed that the rate at which the algae were produced was unaffected by the nutrient concentration, and that the quantities produced were reached at different times (Cushing, 1955). The plastic bag experiments in the Pacific made by McAllister et al. (1960)and Antia et al. (1963)show that such a nutrient limit must be at a very low level, and in nutrients other than phosphorus, as well as phosphorus. A production cycle in the North Sea was shown to be completed with little reduction in nitrate, phosphate or silicate and no reduction in algal reproductive rate (Cushing, 1963; Cushing and Nicholson, 1963); so the decline in algal numbers must have been caused by grazing. This does not mean that nutrient lack never limits production, but that it works as a fail-safe device, rather than as a universal limit ; if grazing animals are absent, production must stop when the nutrients run out. So the very high values of nutrients found in the Antarctic and all over the upwelling areas do not limit production, nor can they accelerate it. The persistence of production in an upwelling area is due not to the presence of excess nutrient, but to the persistent addition of living material from a continuous band of temperate production cycles in the upwelling areas. A remarkable point about the upwelling areas is that phosphorus and zooplankton are positively correlated (Hentschel and Wattenberg, 1930; Holmes et al., 1957; Reid, 1962b) across the south Atlantic and the whole Pacific. Figure 5 from Reid, 196213 shows the distribution in phosphorus and in zooplankton. Figure 5A shows the distribution of phosphate-phosphorus at 100 m in the Pacific and Fig. 5B shows that of zooplankton hauled from about 200 m to the surface. The phosphorus distribution shows high values in the South Equatorial Current from the Peru Coastal Current almost to the Antipodes. The North Equatorial Current is shown in the same way as an arm reaching out westward from the eastern tropical Pacific. Between the two equatorial currents is an area of lower density in phosphorus which may indicate

268

D. H. CUSHTNO

A

FIG.SA. The distribution of PO,-P at a depth of 100 m in tho Pacific Ocean, contoured at five levols from 0-0.25 to 2.OO-tpg atoms/l. (Iteicl, 196%).

the presence of the Equatorial Countercurrent. An interesting point is the very broad spread of high phosphorus values, just east of Hawaii, nearly 30' in latitude. The chart of zooplankton shows much the same structure, but the South Equatorial Current is more prominent, showing the Marquesas divergences. The Equatorial Countercurrent is quite distinctly shown from north of Australia almost to the shores of Costa Rica. An interesting point is the lacuna south of the South Equatorial Current in the eastern tropical Pacific, which appears in analogue off

269

UPWELLING AND THE PRODUCTION OF FISH

B

...:::...:.: ::::::::::jiji

.. .... .....,

50

:.>::::.:.:..

FIQ.5B. The distribution of zooplankton BS sampled with a 1 m net from about 200 m to the surface (with some observat~ionsfrom 300 m and others from 100 m) ml displacement volumr/I 000 m3 (Reid, 190tb).

Baja California. Perhaps the lacuna in the south represents the countercurrent between the Peru Oceanic Current and the Peru Coastal Current. The corrclatioii between phosphorus and zooplankton must,

270

D. H. CUSHINO

be very exact t o be used in a description of oceanic circulation as Reid (1962b) did. The distribution of P04.P at the surface has quite a different character, which cannot be interpreted so easily, presumably because surface phosphorus is less conservative than that at 100 m. Yet that at 100 m cannot be conservative in the sense that salinity is so described. Hence there must be a very profound connection between phosphorus and zooplankton to generate such a correlation in spatial detail. If phosphorus is converted to algae, in its turn converted to animal flesh, one might expect an inverse correlation during a period of time. Then if distance from the coast indicated time from the point of upwelling, the inverse correlation should be obvious in the horizontal distributions of phosphorus and zooplankton-but there is a positive correlation in detail. When phosphorus is used in the production cycle, it is converted to animal flesh, organic residue (dissolved and particulate) and a stock of algae, so the algal population may constitute only a transient component in the system (Harvey et al., 1935). The phosphorus in the water at any point, P,, may be considered as a residue of productive processes, P, < P,, the initial quantity available for production, i.e. the quantity available at 200 m in an upwelling area. Then P, - P, = P,, the minimum quantity used in production. Strictly, we would expect P, to be directly correlated with 8,the quantity of zooplankton ; also, since P, = P, - P,, we might expect an inverse correlation between P, and 8 (provided that enough production had occurred), which is not observed. Let us define P, in more detail, distinguishing that part of production which is locked in the stock of algae, P,, that absorbed into animal flesh, .Pu, and that which is regenerated by animal grazing, BPu. This quantity may consist of two parts : (a) the loss of material into the water a~ the animal eats the algal cells, and (b) excretion by the animals. Then, P, = PT - P, .PU BP,. If we then suppose that BPu > .P, because ,Pu includes the nutrient locked in the zooplankton and note that P, < PR,the correlation between P, and 8 is explained. The quantity of phosphorus excreted must be less than the quantity in animal flesh, but the quantity lost from the daily production in the act of grazing may be high and could itself be greater than the daily increment to animal flesh. Then the observed phosphorus at the surface in the upwelling area would be mainly regenerated phosphorus. If the production cycle in an upwelling area is really a temperate one, then perhaps the observations of nutrients may comprise mainly regenerated material. It should not be surprising because the turnover rate of phosphorus in lakes was shown to be rapid (Hayes and Coffin, 1951); the same processes probably occur in the sea and Cushing and Nicholson (1963)

+

UPWELLING AND THE PRODUCTION OF FISH

27 1

suggested that the turnover rate for phosphorus off the north-east coast of England during the spring outburst amounted to perhaps two or three times a month. In general, the level of nutrients in an upwelling area never reaches the very low level at which the algal reproductive rate might be reduced, from the results of the plastic bag experiments. But progressing offshore, the nutrients do decrease. If the above interpretation is right, this is because the residual quantity of nutrient decreases offshore, as the stocks of algae decrease offshore. Reid's charts of phosphorus and zooplankton extend the correlation to the areas of low algal stock in the centres of the anticyclones, which suggests that the same processes operate there. Then the algal stocks in the deep ocean may subsist on regenerated nutrients. The implication is that the long-established correlation between production and nutrients is a consequence of the dependence of nutrient quantity on production and not the other way round. However, Wyrtki (1964) has estimated the production in the Costa Rica Dome from the decrement of phosphorus during the period of upwelling and has found that the apparent use of phosphorus corresponds fairly closely with the radiocarbon measurements. In the formulation given above P, = P, - P, = BP, - ,P, - P,, which means that the quantity taken up is proportional to that in living material, less regeneration. By analogy with a temperate cycle, regeneration may be low in the rising water, as the production is increasing; then the decrement of phosphorus in the rising water, P,, is proportional to that in living material. A radiocarbon measurement at the surface would be one of A stock, which, if the reproductive rate is constant (i.e. about one division per day), is proportional to stock. So the association found by Wyrtki is an expected one.

IV. DESCRIPTION OF

A

WELL-KNOWN UPWELLINGAREA

A. The California current system The best known upwelling area is that in the California Current, which extends from off Baja California to off Washington State. A special study was executed in the Gulf of Panama, which is not part of' the California Current system (see p. 276). During spring and summer, there is a high pressure system over the Pacific, west of California, and a low pressure system over northern Mexico, Nevada and southern California in the south-western United States, SO winds blow between them, north-easterly, northerly or northwesterly ; and therc are locally very strong winds south of Point Con-

272

D. H. CUSHINQ

ception. The high pressure system intensifies in spring and summer and moves northward (Reid et al., 1958), so the upwelling shifts northward in season. The California Current streams south and is about 350 miles wide and 330 m deep (California, Department of Fish and Game, 1953). Three permanent summer eddies become established : (a) off Cape Mendocino in northern California, (b) south-east of Point Conception, about 100 miles WNW of Los Angeles, from which is constituted the south California Countercurrent, and (c) south of Punta San Eugenio, in Baja California. They are probably generated by upwelling, the southerly eastern boundary current and the local bottom structures. During the period of upwelling, a deep countercurrent ( >200 m) runs from Baja California to a point north of Cape Mendocino and perhaps along the shelf off Oregon (Smith, 1969). When the north-westerly winds weaken, there is a countercurrent inshore, called the Davidson Current (Reid et al., 1958), which has been recognized off the coast of Oregon (Smith, 1969). Lynn (1967) says that the countercurrent in late autumn, winter and early spring runs from central California to British Columbia; a proper upwelling system has been described by Stefansson and Richards (1964) off the coast of Washington State in summer and early autumn. Their work also shows that the effect of upwelling on the coast of Oregon may be masked sometimes by the Columbia River plume. So there is a countercurrent in deep water over the shelf in summer and inshore at the surface in the winter. The California Current starts to leave the shelf off central California and its precursor, the West Wind drift, reaches the shelf north of Cape Flattery. Upwelling occurs south of Cape Mendocino, Point Conception and Punta San Eugenio (Reid et al., 1958). A very rough relation was shown between wind stress parallel to the coast and the upwelling as estimated by the low temperatures inshore (California Department of Fish and Game, 1952). A detailed analysis of the seasonal distribution was made in the years 1949-52 (California Department of Fish and Game, 1953) at thirteen positions between Cape Blanco in northern California and Punta San Juanica in southern Baja California, by months. I n 1949, upwelling occurred in MarchlApril and September along the whole coast ; in 1951 it was restricted to the first half of the year with a slight seasonal shift to the north. In 1951, the upwelling was less intense, with a light spring season and some in OctoberiDecember between Point Conception and the northern part of Baja California. This winter upwelling was probably connected with the intense and widespread upwelling in the following spring, in 1952. These data illustrate the variability of upwclling in time and space and the scasonnl shift north-

WWELLINQ AND THE PRODUCTION OF FISH

273

wards was only just detectable. Off Oregon and Washington, the upwelling occurs in July and August and i t goes on until the winds veer westerly when the Aleutian lows intensify across the North Pacific (Smith et al., 1966). The seasonal shift to the north is shown most clearly in the charts of 13-year mean temperatures by months (Lynn,

1967).

In September 1952, a chart of upwelling in California was constructed in units of ascending velocity (ftjmonth) (California Department of Fish and Game, 1953). Upwelling extended from Monterey, just south of San Francisco, to Ensenada, in Baja California, and a patch occurred off the Cedros Islands north of Punta San Eugenio and off the point itself. Off southern California it was concentratted south of Monterey, south of Point Conception and off Sail Diego ; in these areas and off Punta San Eugenio, the ascending velocity was as high as 200 ftlmonth. There are long-term changes in the patterns of upwelling, as might be expected from the changes in wind speed and direction over long time periods ; before 1949, the upwelling may have been limited to the area between Cape Blanco in southern Oregon and Cape Mendocino and south of Monterey. After 1949, the area extended additionally to Punta San Eugenio, as if the wind had veered a point or so into the

WNW. The biological system has been investigated mainly in the form of extensive egg and larval surveys (Ahlstrom, 1966) between Cape San Lucas, the most southerly point of Baja California, and just north of Cape Mendocino. The distributions of sardine, anchovy, jack mackerel and hake off this coast are well known. The sardine spawns inshore in spring, mainly in the upwelled water ; indeed, since the stock has become reduced, it has concentrated in spawning off Cedros Island and Punta San Eugenio. The anchovy has replaced the sardine since 1951 (Ahlstrom, 1966, 1967) and the eggs are found inshore off southern California and Baja California in all the upwelling areas. The jack mackerel spawning area lies offshore (Blunt, 1969), as if excluded from the points of upwelling, and the hake spawning area (Alverson and Larkins, 1969) spreads over roughly the same region as the sardinej anchovy area. The sardines spawn in late winter and early spring and the hake spawn in March ; the anchovy spawns at about the same time off Baja California, but off southern California it also spawns in the early summer. Alverson and Larkins (1969) have constructed a migration circuit for the Pacific hake. From its late winter spawning ground off California it moves north and appears off Oregon and Washington in June and July. In summer the fish live at about 100 m or less and in winter

214

D. a. CUSHMd

they live in 350-400 m. So, as the upwelling season progresses the fish could ride north in the countercurrent and perhaps return to spawn in the California Current. The extraordinary point is that they spawn in the south when the larvae can take advantage of the upwelling and they migrate north to feed in the upwelling off Oregon and Washington much later on in the year; so the adults live in the upwelling regions for 6 months or more during the year. Although the hake ranges from Cape San Lucas to Kodiak Island off the southern coast of Alaska, it is likely that the stock is retained within the upwelling area by means of the current/countercurrent mechanism. The sardines used to move northward during the summer in much the same way as far as British Columbia. Longhurst (1967) has noticed that during warm years, when TABLEI1 ~~

(a) Engraulidae Clupeidae Carangidae Scorpaenidae Gadidao Scombridae Bothidae Pleuroncctidae (b) Bathylagidae Gonostomatidae Myctophidae

1955

1960

39-9 3.7 3.5 8.6

57.9 1.8 1.1 3-1 6.5 0.3 1.5 0.1 6.5 7.4 10.4

162 0.5 0.5 0-6 5.2

3-8 9- 1

upwelling is less intense, in the period 1957-60, the larvae of the pelagic crab, Pleuroncodes planipes Stimpson, drifted much farther north ; perhaps they were carried north in the inshore surface countercurrent. Thus, from the point of view of the unity of stock, an upwelling area provides mechanisms by which fish can be retained in an extensive region, of about the distances over which fish can easily migrate (500-1 000 miles; Harden Jones, 1968). Ahlstrom’s egg surveys (1969) have yielded a unique opportunity to study the complete community of fishes in an upwelling area. Table I1 shows the percentage of eggs (or larvae) found of the major families. The families are put in two groups : (a) those on the shelf proper, or native to the upwelling area, and (b) those from the deep ocean. It will be seen that the complete list is dominated by the species already described, the anchovy, the hake and the jack mackerel ; the Scorpae-

P

r

P

I

(D

u I

I

I

I

I

I

I

I

I

I

I

I

FIG.6. The relationshipbetween net phytoplankton volume (ml/haul)and the minimum temperature in Monterey Bay, California, U.S.A. (Bolin and Abbott, 1963; Abbott and Albee, 1967).

1

0 rr)

3

B

e 0

h3

l

h

nidae include rosefishes, which are fairly abundant. I n general, the community structure resembles that of temperate waters, with hake for cod, anchovy for herring, roscfish for redfish, jack mackerel for jack mackerel, mackerel for mackerel together with various flatfishes. The bathypelagic fishes are in general found beyond the dynamic boundary at 100 km. The biological mechanisms in the upwelling areas have not been studied specifically. But in Monterey Bay, where upwelling spreads as if from the head of the canyon, the phytoplankton from fine-net hauls have been analysed by months and correlated with the mean minimum temperatures inshore in the bay (Bolin and Abbott, 1963 ; Abbott and Albee, 1967) (Fig. 6). Such a correlation is to be expected, but the fairly long series of observations in Monterey Bay provides evidence of the dependence of the phytoplankton outburst (in the language of temperate production cycles) upon the upwelling system. The study in the California Current was a very extensive one which has yielded many important results on the structure of the current system, the distribution of upwelling and the structure of the biological communities. The dependence of the biological systems upon upwelling has been shown in Monterey Bay, but has been analysed more fully in the Gulf of Panama. B. The System in the Gulf of Panama As part of their study of the biology of live bait, the Inter-American Tropical Tuna Commission has made a comprehensive study of upwelling in the Gulf of Panama, as well as in the Gulf of Nicoya and the Gulf of Tehuantepec, on the western coasts of Central America. For a period of years, observations of wind, temperature, salinity, nutrients and plankton were made at stations in the Gulf of Panama. In general, upwelling is generated by northerly winds blowing from the head of the Gulf between February and April. From changes in temperature, salinity, oxygen and phosphate in response to winds, Schaefer, et al. (1958), estimated that the water upwells at least 50 m each spring. Schaefer et al. (1958) showed that upwelling was limited to the Gulf. The surface temperatures, the reduction of which indicates upwelling, are inversely related to wind strengths from the north 4 days earlier. Forsbergh (1963) estimated that the greater rates of upwelling ranged from 2.1 to 2.8 m per day ; during the period of upwelling the production of radioactive carbon amounted to 680 mg/m2 per day, as opposed t o 330 mg/m2 per day during the rainy period when no upwelling takes place. The radiocarbon observations were significantly correlated with the increase of oxygen and the decrease of phosphate.

UPWELLING AND THE PRODUCTION OF FISH

277

The ratio of radiocarbon production to the quantity of chlorophyll " a '' was used as a very rough index of the rate of production (i.e. A stock/stock) ;this ratio was directly related to light intensity as might be expected, and inversely to temperature at the surface, and so perhaps the algal division rates increase with increased upwelling. Very roughly, the zooplankton was correlated inversely with chlorophyll ; Schaefer et al. (1958) show that the pulse of zooplankton occurs a short time after the algal outburst. The anchovy (Cetengraulis mysticetw) feeds on diatoms (Melosira, Coscinodiscus and Thalassionemu) (Bayliff, 1963) and spawns in very shallow water in November, December and January, just before the main upwelling season in February, March and April (Simpson, 1959). Smayda (1966) has described the distribution of upwelling, showing that it is found around the head of the Gulf, which is roughly the area where the anchovy spawns and where the postlarvae and juvenile fish live on the bottom. The Gulf of Panama is a microcosm and the study of upwelling there illuminates that on the open coasts and in deep ocean. The most significant result is the connection established between wind strength and upwelling, between upwelling and the rough rate of production (as d stock/stock), between algal stock and zooplankton and the spawning of the anchoveta. The detailed mechanisms were not revealed, but the relationships were well established. The results from the two studies, that in the California Current and that in the Gulf of Panama, may be combined. In the Gulf of Panama, the biological links have been established ;the dependence of production upon upwelling (as in Monterey Bay) and the correlation of production rate (as d stock/stock) directly with light and inversely with temperature shows how both rate and quantity of production depend upon the upwelling. Then the zooplankton was correlated inversely with chlorophyll, as if it fed on the chlorophyll, and the anchovy spawns at the head of the Gulf just before the upwelling season, hence the larvae have the best chance of finding food. Similar animals and plants live in the upwelling area off California and the systems must depend upon the upwelling in the same way, and we have seen that the sardines, anchovies and hakes spawn in the points of upwelling at or just before the season of upwelling. But the most important point about the Californian area as a whole is that it appears to be a biological unit. Upwelling and heavy production occur south of certain capes at about the same time every year and the spawning of the fishes appears to be linked to it in time and space. Further, the migration circuits of hake and sardine are linked t o the current system, so that they migrate north to feed in summer and south to spawn in winter.

TABLE 111. AREASOF

BfAJOR

UPWELLINQFROY U.S. NAVY HYDROQRAPRIC OFFICE PUBLICATION 225 (1944) AND OTHERS AS QUOTED Area

Season

(h2)

CALIFORNIA CURRENT Subarea8 Baja California to Point Conception (1) Point Conception to Cape Mendocino (2) Cape Mendocino to Cape Flattery (3)

P E R U CURRENT Subareaa Cape Blanco to 10"s (1) 10cSto Arica (2) Antofagash to Cape Cerranza (1) Cape Carranza to 45"s (2) CANARY CURRENT Subareaa Freetown to Dakar (1) Dakar t o Cape Blanc (2) Cape Blanc to Canaries (3) Canaries to Caseblanca (4) Cape St. Vincent to Vigo (5)

-

F YAMJ J AMJ J AS MJJAS 0

880 560 800

190 190 290

169.103 Sverdrup (1938);Yoshida 106.103 (1955); Reid el al. (1958); 230.103 Wooster and Reid 1963; Stefansson and Richards (1964); California, Department of Fish and Game (1953) (1958)

FMABIJ J A S 0

720 1300 1500 1000

400 170 250 150

288.103 191.103 375.103 150.103

800

50 150 300 150 150

40.103 Berrit (1958,1961, 1962); 105.103 Furnestin (1959);Jones and 306.103 Folkard (1968) 150.103 90.103

-

A S;O

Reference8

FMAMJJA oS D J FMAYJJ N D J EM

-

ONDJ F ONmFBIA AMJ J AS AS J J A S O

-

700

1020 1000 600

Gunther (1936);Posner (1957); Schaefer et al. (1958); Bjerknes (1961);Wyrtki (1966);Wooster and Reid (1963)

BENGUELA CURRENT Subareaa Pointe Noire to Porto Amboin (1) Baia dos Tigros to Walvis Bay (2) Walvis Bay to Orange River (3) Orange River to C a p of Good Hope (4) SOUTH O F CAPE GUARDAFUI Seasom May June July August September October S. SRABIA Seaaona May Ras as Salala to Ras a1 Hadd June Ras as Salala to Res a1 Hadd July Ras Fartek to Ras Hadd August >rukalle 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-

283

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

UPWELLING AND THE PRODUCTION OF FISH

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 (<2 ml/l). It will be shown below that production is high off the Malabar coast during the north-east monsoon, but it is likely that it starts towards the end of the south-west monsoon. In the Bay of Bengal, upwelling has been detected off Walthair in February and March (Lafond, 1954); it probably extends up the coast to Sangor Island off Calcutta in June. Ganaparti and Murthy (1954) have described the circulation during this period in the Bay of Bengal. Under the south-west monsoon, upwelling probably occurs all along the coast of Orissa, which lies parallel to the direction of the south-west monsoon. Yet, as will be shown below, high production also occurs on the Orissa coast during the north-east monsoon. Between December and January, upwelling is found in the Andaman Sea (Lafond, 1957 ; Wyrtki, 1961) between the coast of Burma and the Andaman Islands and off the west coast of Thailand. There is upwelling off the coasts of Ceylon which appears in Fig. 14, p. 297 from Kabanova (1968). It also occurs in the shallow Gulf of Thailand, on the west coast in August and on the north-east coast in October and January ;slight upwelling occurs all the year round at 12"N and 101"W. Off South Vietnam, upwelling takes place during the summer monsoon between the central South Vietnamese coast at Nhatrang and a point some hundreds of miles up the coast (Wyrtki, 1961). Wyrtki (1961, 1964) and Rochford (1962) have described upwelling areas off Java and north-west Australia, and in the Flores, Banda and Arafura Seas ; those off north-west Australia and in the East Arafura Sea occur in July and August but are little understood in the distributions of properties. The evidence for the Indonesian areas is based on certain sections in the absence of charts of surface temperature at the right season.

UPWELLING AND THE PRODUCTION OF FISH

291

D. The equatorial system The physical structure of the equatorial system has been briefly described in an earlier section. Figures 5A and BB, p. 268 show the distribution of phosphorus a t 100 m and of zooplankton (Reid, 1962b), and Fig. 13, p. 295, the distribution of radiocarbon (Koblentz-Mishke, 1965) in the Pacific. The distribution of radiocarbon shows high productivity along the region of the undercurrent a t the equator from 140"W to the Galapagos Islands. I n contrast the phosphoruslzooplankton distributions do not show the undercurrent but the broad pattern of the North and South Equatorial Currents. Presumably the zooplankton distributions represent an integration over a period of time and the zooplankton which might have been produced above the undercurrent becomes dispersed during that period in the waters of the South Equatorial Current. Another important point about the equatorial system is the divergences in the eastern tropics, in the western tropics and in the North and South Equatorial Currents. The eastern tropical systems between the two currents form grcat rich triangular areas between California and Peru, and between Dakar and the Congo, extending hundreds of miles to scaward. Mr. C. Bowley has told me (and see Bowley et al., 1969) that the eastern tropical Pacific area of rich production can be picked off satellite photographs. Dark spots are seen in the upwelling areas which become bright as the satellite passes overhead and then become dark again as the satellite starts t o set. These spots are distributed above the Cromwell Undercurrent and up to a fair distance off the coast in the California Current. Their physical structure suggests that they are patches of calm water and their association with the undercurrent suggests that the phytoplankton is rich there. There are areas of divergence in the eastern tropical areas of each ocean on the edges of the equatorial currents and across the domes. The area off West Africa is most interesting at this point, for the Guinea Dome (Mazeika, 1967) is extensive, and there is a special coastal upwelling off Ghana and the Ivory Coast (Berrit, 1962) with an area of divergence in the South Equatorial Current south of it. Because the coastline runs westerly not very far from the equator, the northern dome is displaced north-westwards and the areas of coastal upwelling and of divergence lie about the equator not too far from the coast. Figure 5B, p. 269, shows that thcrc are rich patches of zooplankton off New Guinea and the Philippine Islands, which correspond t o areas of divergence there as noticed by Hidaka and Ogawa (1958) (see Fig. 20, p. 322). Further, there is an extensive area of divergence also reflected

202

D. H. CUSHINQ

in the zooplankton distributions in the South Equatorial Current in the region of the Marquesas Islands. From Fig. 5B, showing the zooplankton distributions, it is also possible to see where the Equatorial Countercurrent runs, at about 5-8"N, where there is a long rib of low density right across the Pacific. This is not surprising, for in general the countercurrent is a region of convergence at most seasons (Hidaka and Ogawa, 1958). In the northern summer there are convergences along nearly the whole length of the Equatorial Countercurrent ; the same is true during the winter, but the convergences are broken by patches of divergence in the west. In the southern summer there are extensive divergences in the South Equatorial Current ; in the North Equatorial Current, in the northern summer, there are also divergences, but they are less extensive, indeed less than in the northern winter.

5'

s

0"

5"

10"

15'

20' N

Fro. 12. Section of the Costa Rica Dome, in phosphorus (pg.atoms/l) (Cromwell, 1968).

E. Domes and the eastern boundary currents The classic dome is the Costa Rica Dome at 7-5-9-OoW (Wyrtki, 1964) formed as the Equatorial Countercurrent turns back into the North Equatorial Current. A vertical section across the structure shows a dome-like appearance as the thermocline, together with other properties, rises towards the surface. Figure 12 illustrates phosphorus content in a section across the Costa Rica Dome (Cromwell, 1958)from south to north. The Countercurrent lies between 5"N and 8"N and the North Equatorial Current at 12ON and the base of the dome is observed between 100 and 400m. It is most prominent when the Equatorial Countercurrent is strongest, in late summer and in autumn, but it exists at all seasons, even in February and March when the countercurrent appears to be absent ; so perhaps the structure is a little more complex than stated above. The countercurrent turns north into the Costa Rican Coastal Current and then westward into the North Equatorial Current. The dome arises in the centre of the eddy, and with the fluctuations in current strength the shape changes and domelets may

UPWELLING AND THE PRODUCTION OF FISH

293

be split off. Upwelling is generated on the left flank of the anticyclonic flow and by a lateral transport across the dome (Wyrtki, 1964). Consequently there must be a sinking on the right of the flow, shown most prominently in a hollow south of the dome, as part of the countercurrent turns south and then west into the South Equatorial Current. Wyrtki (1962) has shown that the upwelling off Java and Sumbawa is a dome analogous t o the Costa Rica Dome ; there is an Indian Ocean Countercurrent, but it is more temporary than the Pacific one, because of the switch from one monsoon t o the other. The dome off Java and Sumbawa lasts only from May to September during the south-east monsoon, in the southern winter. The domes in the eastern tropical Atlantic are described by Mazeika (1967). From January to April, in the southern summer, there is a dome off Angola, the Angola Dome. Similarly from July to September, in the northern summer, there is a dome south-west of Dakar, the Guinea Dome. It is formed as the Equatorial Countercurrent turns into the North Equatorial Current as an extension to the Canary Current ; in other words, it is an exact analogue of the Costa Rica Dome but is seasonal, like the Sumbawa Dome, presumably because the Equatorial Countercurrent in the Atlantic is less strong than that in the Pacific. The Angola Dome cannot be formed in the same way but it has a cyclonic circulation ;perhaps it is generated by the turning of the undercurrent into the South Equatorial Current. Mazeika also shows that there is a dome just south of the equator between SOW and 3'E, which is a divergence generated by the easterly winds offshore off the upwelling area off Ghana and the Ivory Coast. The area of the Costa Rica Dome is 1-5.105km2. That off Java is given as 3. lo5 km2, taken from Wyrtki (1964). The Angola and Guinea Domes are possibly a little larger than that off Java. The area of the Guinea upwelling is set provisionally as 1.105 km2, from the length of coastline (10') and a distance offshore of 160 km (Mazeika, 1967).

F. Minor upwellings The upwelling in the Gulf of Panama has already been noted. Similar upwellings have been found in the Gulfs of Nicoya and Tehuantepec; in the latter there are northerly winds of exceptional severity, the Tehuantepequeros, which draw the water up as quickly as 10 m/day (Roden, 1961). Redfield (1955) described an upwelling in the Gulf of Venezuela; Richards (1960), Curl (1960) and Fukuoka et al. (1964) produced evidence of upwelling and high productivity shoreward of the Cariaco Trench, east of the island of Santa Margarita and in the Gulf of Cariaco in Venezuela. Garner (1961) has described coastal upwellings

294

D. H. CUSHINO

off Cape Reinga and off the north-east coast of the South Island of NCW Zealand. There are upwellings off thc coast of Yucatan in Mexico and the north coast of Cuba (Bogdanov el al.,1968; Khroinov, 1966b).

VI. THE PRODUCTION OF LIVINGMATERIALIN UPWELLING AREAS

THE

There are many estimates available from the upwelling areas of primary production, using the radiocarbon technique, and of the stock of zooplankton, using common nets. The number of observations is enough to establish a mean value for an area throughout the season, but there are never enough to show the nature of a seasonal trend within the upwelling area. The total primary production of an area is given by raising the mean radiocarbon values as gC/m2 per day by area and duration of the season. An attempt is made to estimate the production of the zooplankton, knowing the stock and the generation time, and it is also raised by area and the number of generations in each season. From the two estimates, of primary production and of secondary production, the one of tertiary production is derived by taking 1% of the first and 10% of the second.

A. Primary production The radiocarbon method of estimating primary production has been used extensively since its introduction by Nielsen (1952). Since the question of respiration in radiocarbon measurement was resolved by Nielsen and Hansen (1959) many of the doubts raised about the method during the fifties have disappeared. However, Nielsen (1964) and Goldman (1968) have shown that the earlier method of calibration was at fault and that most of the measurements made so far have to be raised upwards by a factor of 1.45. With the introduction of scintillation methods, the radiocarbon method has become an absolute one (Wolfe and Schelske, 1967) rather than a relative one, and there is no need for the old method of calibration. The measurements in the Canary Current upwelling (Lloyd, 1970) were made with scintillation counters and SO are not raised by 1.45. Koblentz-Mishke (1965) has combined the surface observations (in mgC/m3per day) with those made at a number of depths in the photic layer (in gC/m2 per day) and her regression has been used to convert many surface observations in mgC/m3 per day to gC/m2per day. Provided that enough observations are available, an annual mean production waa estimated for each area, or subarea. The data were taken from Steemann Nielsen and Jensen (1957-59) (from the “ Galathea ” Expedition in the Atlantic and Indian Oceans), Ryther et al. (1966) (from the “Anton Bruun ” voyage during the

UPWELLINQ AND THE PRODUCTION OF FISH

290

FIQ.13. Distribution of radiocarbon measurements in the Pacific Ocean in gC/ma per day (Koblentz-Mishke, 1965). ( I ) 100; (2) 100-150; (3) 150-250; (4) 250-650; (5) 650 mgC/m*.

International Indian Ocean Expedition), Kabanova (1 968), Holmes et al. (1957), Forsbergh and Joseph (1964), Corcoran and Mahnken (1969) and Lloyd (1970). The summaries of Pacific Ocean data in Koblentz-Mishke (1965) for the Pacific, in Blackburn (1966) for the eastern tropical Pacific and in Angot (1961) for the western Pacific have been used extensively as have those of Wooster et al. (1967) for the Arabian Sea and Kabanova (1968) for the Indian Ocean. Doty (quoted in Angot, 1961) made many measurements in the Indonesian region, which are considerably higher than those made by Nielsen and

296

D. H. CUSHINO

Jensen and Angot in the same region; as tlic reason for the higher values is obscure, they have not been used. Figure 13 gives Koblentz-Mishke's production in thc Pacific in gC/m2per day. The high latitude divergences (at latitudes >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 (<0*3 gC/m2 per day) includes all subareas in the California Current, the Costa Rica Dome, the two subareas off Chile, one in the Benguela Current, that in the Marquesas divergence, off New Guinea, off the Andaman Islands and off north-west Australia.

TABLE IV CARBON PRODUOTION AT THREE TROPHIC LEVELS

Area and duration of upwelling A

B

Secondary production

Primary production

C

D

1

F

G

n-..I.-.-

H TI-I.....

J

K

-

Carbon (tons. ~ u r1061yr, uur' Displacement Depth " u'ur'cB beneath Stock Generation (tons. 10B,,yr, volume sampled ( m ) Area Duration oclm2/d 1 ma (gC/m2: 1 time (days) ( k d .103) (days) (as observed) 1.45) rounded (mll1000m3) (or bottom) (,.,"-,.," ml/m2\ ".p ,D"I ,

Pacifc California 1 2 3 Costa Rice Dome E. Tropical Peru 1 2 Chile 1 2 Marquosas New Guinea

11.03 4.45 15.01 16.73 1245.55 3644 76.27 35.53 8.03 514-46 41.04

10

169 106 230 148

180 180 180 300

0.250 0.161 0.250 0.260

288 191 375 150 8 760 460

270 270 270 180 300 300

0.325 1.020 0.242 0.205 0.135 0.205

40 105 306 150 90

150 205 180 180 150

0.400 0.390 2.087

3.48 12.19 114*95*

3 10 75

8.10

10

100 35 240 210 144

120 90 240 360 240

0.600 0.500 0.600 0.280 1.130 0.530 1.560

7.20 3.46 94-38 98.60 78.15

10 3 100 100 75

Indian 95 Somali 131 S . Arabia 112 Malabar Madagascar Wedge 1 014 NE Madagaqcar 72 Orissa (SW monsoon) 96 Orissa (NE monsoon) 96 Andaman 100 W. Ceylon 10

180 180 150 180 120 150 120 90 300

0490 1.000 1.000 0.750 1.100 0.4 15 0.620 0.225 0.410

17.10 34.19 1640 8-60 9.50 8.67 12.92 3.42 1.14

Indonesia etc. Java NW Australia E. Arafura Flores Banda Gulf of Thailand Vietnam

150 150 120 120 120 150 120

0.4 15 0.284 0.390 0.505 0.650 1.298 1-270

27.09 18.53 16.97 8.79 11.31 20.75 44.20

Atlantic Canary

1 2 3 4 5 Guinea Dome Guinea Benguela 1 2 3 4

300 300 250 100 100 75 200

* This figure is not raised by 1.45.

5 15 15

35 75 35 10 35

28 42 70 43

1.82 2.73 4.55 2.80

225* 200 150 142 75 150

140 140 140 300 300 300 300 300 300 200 200

68 60 45 150 25 30

4.42 3.90 2.93 2.84 1.63 1.95

375 266 533 280

200 200 200 200

75 53 106 57

4.88 3.45 6.89 3.71

200 300 500 144

L

Tertiary p r o d u c t h

Ml

Nl N2 (MllD) (M2lD) X 1.33) Transfer Transfer (Ml Carbon coM2

0

Pl

pa

Qi

Q2

Rl

RZ

(cl2)(-i-) *

Number (,D~ 0 . 0 1 ) (O.lM1) (O*lMa) 4(Q1 Wet x 7.47) Wt (Qa x 7.47) of Carbo; COCarbon Carbon Carbon Wet Wt gener- (tons.10 /yr) Carbon (tons.106lyr) efKient eficient (tom.104lyr) (tons.104/& (tons.1 0 4 1 ~ ~ ) f2arbon (tone. 106/yr) (tons. 106/yr) ations (tow.1 0 4 1 ~ ~(tOn8.104/yr) )

(%)

52 61 68 31 31 52 52 52 68

3.46 2.95 2.65 9.67

52 52 61 61

1.41 1.13 3.68 5.32 92.01

5.18 5.18 5.18 2.65

1.06 0.85 2.77 4.00 69.18 6.59 3.86 5.69 1.13

2.89 3.94 2.95 2.95

0.56 1-43 6.22 1.64

0.75 1.90 8.27 2.18

8.76

5-13 7.57 1.50

(%I

9.6 19.1 18.45 23.9 5.54 17.99 5.06 16.02 14.00

12.8 25.4 24.5 31.2 7.39 23-90 6.64 21.32 19.70

11.03 4.46 15.01 16.73 1346.55 36.64 76.27 35.53 8.03 ~114.46 41.04

16.1 11.7 5.4

21.5 15.6 7.2

3.48 12.19 114.95

10.6 8.5 27-7 40.0 691.8 65.9 38.6 56.9 11.3

14.1 11-3 36.8 53.2 920.1 87.6 51.3 75-7 15.0

10.8 6-5 21.4 28.4 (968-7 51.3 57.4 46.2 9.5

12.6 7.9 25-9 35.0 1103.1 62.1 63.8 55.6 11.5

0.81 0.49 1.60 2.12 72.36 3.83 4.28 3.45 0.7 1

0.94 0.59 1.94 2.62 82.40) 4-64 4.77 4.15 0.86

5-6 14.3 62.2 16.4

7.5 19.0 82.7 21.8

4.6 13.2 88.6

6.5 15.6 98.8

0.34 0.99 6.62

0.41 1.17 7.38

15.9

21.2

11.5

14.2

0.86

1.06

108.0 71.1 23.6

144.0 94.6 31.4

101.2 84.8 50.9

119.2 82-3 54.8

7-66 6.34 3.80

8.90 6.15 4.09

17.10 34.19 16.80 8.66 9-50

12.2 24.7

16.2 32.9

14.6 29.4

16.6 33.5

1.09 2.20

1.24 2.50

22.7

8.67

14.8

19.7

11.7

14.2

0.87

1.06

12.92 3.42 1.14

2-0

2-7

2.7

3.0

0.20

0.22

26.4 21.2

35.1 28.2

26.7 19.8

31.1 23.3

2.00 1.48

2.32 1.74

8.10 315

200

63

4.10

31

3.87

1.59

2.12

22.1

29.9

750 375 320

200 200 200

150 75 64

9.76 4.88 4.16

52 52 61

4.62 6.93 3.94

10.8 7.1 1 2.36

14.4 9.46 3-14

11.4 7.2 3.0

15.2 9.6 3.9

15 35 15 10 10 10 15 3 3

250 250 114 530

200 200 200 200

50 50 28

48 31

3.75 5.80

1.22 2.47

1.62 3-29

7.0

106

3.25 3.25 1-50 6.89

213

200

43

2.80

1.97

17.1

200

10

0.65

5.36 4.28 2.90

1.48

50

28 28 31

35 15 15 10 10 15 35

140 117

200

28

1.82 1.50

31 31

4.84

too

23

4.84

7-23

9.1 9.63

0.20

0.27

6.0

8.0

2.64 2.12

3.51 2.82

9.8 11.4

13.0 15.2

7-20 3.4 6 94-38 98-80 78.15

27.09 18-53 16.97 8.79 11.31 20.75 44.20

C 51.64

58.74

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UPWELLING AND THE PRODUCTION OF FISH

301

Again the major upwellings are also the most intense, but most of the less intense ones appear to be in the Pacific. An important point is that the intensity of production in the upwelling areas is greater than elsewhere in the tropics or subtropics. A glance at the distribution of the intensity of production in the Pacific and Indian oceans (Figs. 13 and 14) shows that the intensity of production in theupwelling areasranges from O.l-l.OgC/ma per day (and some observations are higher still), whereas outside them the intensity tends to be less than 0.1 gC/m2 per day. Effectively, in magnitude, this is the comparison between the high amplitude discontinuous production cycle of high latitudes and the low amplitude quasi-steady state one of low latitudes. B. The production of zooplankton At the present time, the estimation of secondary production is difficult because the dependence of the duration of the life stages of various invertebrates (primarily copepods) upon temperature is only known sketchily. It is true that this relationship has been established for a few species, but a generalization is needed for a proper application. Further, we need t o distinguish between the forms of production, with perhaps a single generation in high latitudes, from those with many generations which may be common in the upwelling areas; John Gulland has suggested to me that the important factor might not be the generation time but a fraction of it depending on the mortality rate, if the secondary production were continuous. The material available is only the simplest, an estimate of stock as sampled by some simple nets, the constructions of which are common. Because the season of upwelling has been defined in an earlier section, the duration of the season can be divided by the generation time and so the average stock is raised by the number of generations, yielding the roughest estimate of production. One of the standard nets is the metre net which has been used extensively by American organizations. The mouth is 1 m in diameter, the mesh size is about 0.25-0-31 mm and the net is hauled vertically from about 200 m at a speed of about 1 m/sec. The Indian Ocean net is a very similar net, with a mesh size of 0.33 mm ; off southern Arabia, it was hauled in strong winds and a wire angle of 45" has been assumed (from my own observations on R.R.S. " Discovery "). The Russians working in the Indian Ocean have used a large Juday net, 0.5 m2 in area, with a mesh size of 0.26 mm ;they express their results as mg wet wt/l 000 m3, which is essentially the same form of expression as used in the American and Australian work (ml/l 000 m3). Tranter (1962) has described the form of net used off north-west Australia and off Java. Trantcr ( 1 063) has shown that the Juday net with a mesh of 0.26 mm

302

D. H. UUSHING

catches more material than the Indian Ocean net, but it was not stated whether the additional material was of nauplii or of algae ; however, a correction factor for converting catches of the Juday net t o the 1m was derived. From such nets, a proportion of the zooplankton population escaped through the meshes and a further proportion evaded capture, and it is likely that the displacement volume included an unspecified volume of algae. There is no information on the mesh selection of these nets in terms of displacement volume of animals of different sizes. It is hoped that the loss of zooplankton through the meshes is balanced by gain of algae and nauplii by clogging ; so the low volumes might be underestimated and the high ones might be overestimated. Loss by escape has not been measured for nets of this type, although it has been shown for some larger animals (Fleminger and Clutter, 1965; McGowan and Fraundorf, 1966), so it is possible that euphausids are improperly sampled. However, as sampling was carried out both by night and day, it is possible that the underestimate is not too great. At the present stage of zooplankton sampling, the nets used probably represent the best compromise for estimates of zooplankton displacement volume over extensive areas. The best way would doubtless be to count the animals and estimate their volumes from an array of nets, each sampling a band of sizes properly. But the labour for treating the very large number of samples would never become available. Many expeditions have sailed over the Pacific Ocean in the last two decades. The zooplankton hauls are well summarized by Reid (1962b); those in the very rich area in the eastern tropical Pacific have been analysed by Blackburn (1966). Most hauls were made from about 200 m to the surface (but some were hauled from 100 m and some from 300 m), Observations in the Peru Current have recently been confimed with large quantities of information on Hensen net hauls from 50 m t o the surface. During the International Indian Ocean Expedition, the Indian Ocean net was hauled through a water column of 200 m. I n the Atlantic Ocean, zooplankton operations in a standard way are lacking. Frontier (1963) hauled a Hensen net (0.33 ma; 0.41 mm mesh) in the Guinea Current off Abidjan; with the same net, Mensah (1969) has described in some detail the seasonal cycle in the continental shelf off Ghana, i.e. in the Guinea upwelling. There are a few observations made off Cap Blanc in the Canary Current (Khromov, 1962; Pavlov, 1968) with a Juday net. Between Dakar and Freetown, Khromov (19658) has recorded some observations during the early upwelling with a Juday net. Elsewhere in the Canary Current and in the Benguela Current, the best observations were those made on the " Meteor " expedition. On that expedition, numbers of " metazoa " were counted from 4 1. of water

UPWELLING AND THE PRODUCTION OF FISH

303

taken at thc surface, at 50 m and at 100 m (Hentschel, 1033). Kamshilov’s ( 195 1) formula converting length to weights for copepodites (0.6-1.0 mm) and nauplii (0.08-0.10 mm) has been used. This procedure yields results which are comparable with those from other upwelling areas. Most of the observations of zooplankton stock are expressed as ml/l 000 m3 displacement volume (in American usage) or mg/m3 wet weight (in Russian usage), and in this paper they are treated as being the same. As the nets are hauled from specified depths the quantity per cubic metre can be readily converted to a quantity beneath a square metre. In the upwelling areas the nets have been hauled usually from about 200 m, which is approximatcly the depth of the upwelled water. It is possible that some animals, for example euphausids, rise from deeper water into the upper 200 m at night, in which case the stock is underestimated to some extent. An upwelling area might be 800 km in length by 200 km in width (in the biological sense) ; a part of it contributes to a current flowing towards the equator at about 20 km/day (Wooster and Reid, 1963), which means that water passes through the area in about 40 days. There is thus an input of zooplankton from the poleward end, which has been generated in the divergences further away. Very roughly, it takes one zooplankton generation for water and zooplankton to be drifted across the length of an upwelling area. Any mature copepod reaching an upwelling area would ensure a high survival rate for its offspring in the high algal production there. But plankton animals are probably also generated within the water which has risen from below, and because of the mixture between the two potential sources it may be idle to distinguish between them. We may consider the production of zooplankton to be autonomous within the upwelling area only, because there may be one generation within the drift time across the area. The upwelling scason may last for many months in some areas and the production of zooplankton is given by the average standing stock as ml/m2, multiplied by the number of generations during the upwelling season. This is a fair estimate if the generations are discontinuous, as they are in temperate waters, but if breeding goes on all the time, the measure of a generation for production purposes is not the interval between the appearance of mature adults, but is something less, depending upon the mortality. From the structure of the production cycle in thc upwelling area, such an effect might be expected, but no evidence is yet available on the possible mortality rate. Marshall and Orr (1956) give thc duration of copcpodite stages as a proportion of the duration of oopepoclito stagr I. McLaren (1 965) has

304

D. H. UUSHING

published durations of some copepodite stages at different temperatures and so a relationship between stage duration and temperature was constructed. Marshall and Orr (1955) also provide some data on the duration of maturation and of hatching and so the length of a full generation can be roughly worked out at different temperatures. It is not a very precise estimate, but it does not differ very much from the estimates of Heinrich (1961). The generation time estimated in this way has been arbitrarily lengthened by one-third to take account of the intermittent character of upwelling, due to variation in wind stress (California Department of Fish and Game, 1953). The zooplankton distributions off California (Thrailkill, 1956, 1957, 1959, 1961, 1963) reflect the transient structures of an upwelling region, possibly because the animals are vulnerable t o food lack in the periods between upwellings. The same procedure should really be applied to the algal production, but a short halt of a week or so would only reduce the rate of increase of production (and of course is taken up in the average radiocarbon estimates), but it might cause the local failure of a brood of nauplii. Then when upwelling returned, it would take half a generation for the new brood t o get under way. The estimate of one-third of a generatjon was taken from the seasonal picture of intermittent upwellings off southern California (California Department of Fish and Game, 1953) but there is no evidence of the real dynamic effect upon the secondary production. I n Table IV, the secondary production is estimated in two ways, with and without the lengthened generation time. It is possible that the intermittent halts in the upwelling process (which are not confined to the California Current) really sustain greater levels of production. The rate of increase of algal production is temporarily halted and the zooplankton production is perhaps stopped. When the upwelling is resumed, the rate of algal production is resumed, but the grazing restraint on the populations is absent. Consequently, during the delay until the grazers grow again, a form of algal outburst takes place. Hence a considerable degree of patchiness in time and space is generated. Ivlev (1961) showed that animals convert, and grow more effectively, on food which is distributed in a patchy way, than on food which is distributed evenly. Thus the effects of intermittent upwelling on the possible destruction of the zooplankton may be mitigated by the manner of their exploitation of the algal production. There is no evidence t o support these speculations. Lovegrove’s (1962) data show that copepods, dried to a constant weight, contain 5.6% of carbon ; Beers (1966) found the same value for copepods, but 5.8% for pteropods, 6.4% for euphausids and 6.7%

for other Crustacea ; Lasker (1966), however, found a higher value for euphausids, 7.2%. If we assume that displacement volume is a fair estimate of wet weight, then a factor can be used to convert displacement volume as d / m 2 t o gC/m2. The correct conversion factor depends upon the relative distribution of copepods and other forms in the zooplankton ; sometimes copepods will predominate and sometimes euphausids, in which case the factor will shift from 5.6 to 7.2%. An approximation of 6.5% will be used. The estimate of carbon in the secondary production is given, for example, in the fist line of Table IV: 1-82 gC/m2 x (169 km2.lo3 x lo6 m2) x 3-46 gen = 0.106.106 tons C/year.

tons C/year

The results are given in column M, ; in column M,, the quantities are raised by 1.33, t o take into account the possible halt to zooplankton production caused by intermittent upwelling. Columns N1and N , give the transfer coefficients, which are the ratios of secondary production to primary production, calculated as M,/D or M,/D. These coefficients are analogous to Slobodkin's ecological efficiency (1959), which is the ratio of yield from one trophic level t o that from a second trophic level. I n column M , is tabulated the secondary production in tons C.106/year, where the annual production is considered as occurring only in the upwelling season ;of course, some production occurs in such areas outside the season of upwelling, and in one case, at least, off the Orissa coast of India, there is some production during both the northeast and the south-west monsoons, but that during the north-east monsoon cannot be generated by coastal upwelling in the ordinary sense. The greatest production (>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).

UPWELLING AND THE PRODUCTION OF FISH

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

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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

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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).

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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).

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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

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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

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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

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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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D. € CUSHINQ I .

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

”.

( 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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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 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.”

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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

?

L

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

Andhra coast

Name of shipworm

No.

Madras coast

--

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

-

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

X X X X X X X X X X

X X

X X X X X X X X

.

.

-

x present;

- not recorded

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

THE BIOLOGY O F WOOD-BORING TEREDINID MOLLUSCS

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<.

.

T.pormricrrmia Cla;,p . 2N. T.somerei Clapp 19. T . trirriigulrtria Edmontlsori 4’1.

.

30. Lyrmlua riffiitis (Dwhayrs) . 31. L . bip~rrtitcr(Jeffreys) 32. L . mtt880 (Lam).) . 33. 1,.iitediolo6ntn (Eclrnontlson) 34. L. pedirellrrtus (Qriatrrfages) (Hoch) . 35. L. tr~hoioshiit~etisis 36. Nototeredo edur (Hetllry) . 37. X. knosi (Bartsch) . 38. N. ttorrtrgirn (Sprriglrr) . 39. &‘prlhoteredo obtuan (Sivickis) 40. S. s p t h t i (Jeffreyn) , 41. ,I’crueitorn dryas (Dall) . 42. N. duiilopei Wright 43. K. excolpn (Bartsch) . . 44. K.fusliculcr (Jeffreys) 45. S . hedleyi Schepmen . 46. Boilkin niierhoeiinis Roch 47. B. nuatrrrlia Cdman . 48. B. borthelowi Bartsch . 49. B. bipnlmulntn (Lamarck) . 50. B. bipetinntn (Turton) 51. B. brecis (Deshayes) . 52. B. rnmpinellntn Moll C Hoch 53. B . ccirinata (Gray) . 54. B . riebn Clench & Tiirnrr . 55. B . clestrurtrr Clench C Turnrr 56. B. fimbricrtula Moll & Roch 57. B. fosteri Clench C Tiirnrr 58. B. gouldi (Bartsch) . . 59. B . grncilis Moll . 60. B. mnrtensi (Stempell) . 61. B . itordi Moll . 62. B. orcutti Bartsch . 63. B. philippiiwisis Hartsch . 64. B . rorhi Moll . 65. B. aetnceo (Tryon) . 66. B. zeteki Bartnch .

.

. .

348

N.

BALAKRISHNAN NAIR AND M. SARASWATHY

Fro. 1. Teredo norveggica ( =Nototoredo norvagica). Entire animals removed from their burrows.

of the Eulamellibranchia. This sub-order is characterized by the presence of a tubular mantle, a discoidal foot, a reduced hinge, a small internal ligament, a large posterior adductor muscle and a much smaller anterior adductor yuscle. The shells are highly specialized drilling tools with a large pkydal gape, a denticulated anterior, outer surface, a pronounced dorsal and (except for the Pholadinae) ventral articulating faces on which the valves rock. Stylloid apophyses are present (except in Xylophaginidae and Jouannetiinae) extending from beneath the umbones and providing surfaces for the insertion of pedal muscles. The greatly reduced shell, the absence of accessory plates for the shell and the presence of curious structures called pallets are characteristic of the Teredinidae and in these respects they differ from the Pholadidae. As stated above, the shell of the Teredinidae functions as a drilling tool. The naked body projects far beyond the posterior margins of the shell valves. But the only visible parts of the shipworm in its natural condition are the two relatively small siphons at the posterior end of the body used for the inlet and exit of the respiratory and feeding current of water. These are extended (Fig. 2) through small holes which represent the points of initial entry of the molluscs into the wood. Covering only a small portion of the anterior end of the visceral mass, the shell accommodates within it only the discoidal foot, the anterior part of the alimentary canal and the adductor muscles. The

349

THE BIOLOQY OF WOOD-BORINQ TEREDINID MOLLUSCS

FIU. 2.

An underwater photograph of the displayed siphons of Teredo megotava (= Psiloteredo megotara).

shell valves gape widely both in front and behind for the projection of the foot and the extension of the body respectively. The edges of the shell are not brought together because of the modified contact on the dorsal and ventral articulations. Figure 3 shows the general arrangement of the organs in a typical shipworm Bankia indica ( B . carinata) as seen from the right side with the shell and mantle removed. In general this description holds good for such species as Teredo navalis, T . furcifera, T . pedicellatus, Bankia gouldi and Bankia setacea. Owing to the lengthening of the body, the visceral mass occupies approximately a third of the animal while the ribbon-like posterior part of the ctenidium (G)extends from the visceral mass to the base of the siphons (ES, IS). Most of the organs lie behind PA

Fro. 3. Bankia indica (=B.carinata). The general disposition of the organs in the mantle cavity as seen from the right side. AA; anterior adductor, AAO, anterior aorta; AC, anal canal; AN, anus; APC, anterior part of the ctenidium, ARD, afferent renal duct ; AU, auricle of the heart ; CAC, caecum of the stomach ; CH, cephalic hood ;CO, collar of the mantle ;CTI, coiled typhlosole of the intestine ;DD, digestive diverticula; ERD, efferent renal duct ; ES, exhalant siphon; F, foot ; G, gill; MG, midgut; I, intestine; IBC, infra branchial cavity; IS, inhalant siphon; K, kidney; LP, labial palp ; M, mouth ; OV, ovary ; OVD, oviduct ; PA, posterior adductor; PC, pericardium; POA, posterior aorta; R, rectum; SBC, supra branchial cavity; ST,stomach; V, ventricle; VG, visceral ganglion.

350

N. BALAKRISHNAN NAIR AND M. SARASWATHY

the posterior adductor muscle (PA) instead of anterior to it as in most bivalves. The discoidal foot (F) occupies the anterior-most portion in relation to its use as an organ holding the shell in position while boring. The pericardial cavity (PC) with the contained heart has not only considerably elongated but has also undergone rotation around the posterior adductor with the result that it lies above the intestine. Associated with these, the relation of the various parts of the circulatory system has changed. The posterior aorta (POA) continues in front of the ventricle while the anterior aorta (AAO) proceeds backwards. The kidney (K) and ureters come to lie on the upper side of the pericardial cavity and ventral to the anal canal (AC). The gonads are creamy white conspicuous bodies situated in the midline dorsally and laterally. The renal and reproductive openings have shifted back as also has the visceral ganglion (VG). The digestive organs have not rotated like the pericardium. The cylindrical stomach (ST) is surrounded ventrally and posteriorly by the irregular tubules of the digestive diverticula (DD), the capacity of the stomach being greatly increased by the long cylindrical caecum (CAG), and the intestine (MG) extending posteriorly around the caecum as a long loop. The mouth (M) and the anus (AN) retain their usual positions, the former between the anterior adductor and the foot, the latter on the dorsal side of the posterior adductor. The mantle cavity extends behind as a long cylindrical canal accommodating the ctenidia. The distal end of the tube is produced into the siphons. The pallets (Fig. 4) are situated at the base of the siphons on either side beneath the muscular collar and are provided with muscles which control their movements. The two pallets are pressed against each other so that the straight inner sides become apposed and the semicircular outer surfaces form a complete conical plug effectively closing the circular opening when the siphons are retracted within the burrow. If the salinity of the sea water should change greatly, or if poisons are introduced or the timber is taken out of water, the pallets are thrust into the opening, closing the burrow and protecting the soft animal inside. The retraction and protrusion of the pallets are brought about respectively by sets of retractor and protractor muscles. The adductors of the pallets facilitate the separatioxl of the right and left blades of the pallet prior to retraction of the pallets which enables the siphons to extend. I n Bankia the pallets consist of a series of funnel-like cone-in-cone structures which constitute the blade. These have been secreted and cemented in succession to a calcareous cylindrical handle. The cone-in-cone units of the blade are not of the same size, the largest one being found towards the base and the smallest at the tip, the blade tapering from base to tip. They

THE BIOLOGY O F WOOD-BORING TEREDINID MOLLUSCS

RP

APA

351

pp

Flu. 4. The siphon and pallet apparatus of Banlcia (Balakiella) gouldi Baxtsch (after Sigerfoos, 1908). APA, adductor muscle of pallet ; CO, collm; ES, exhalant siphon ; IS, inhalant siphon; PA, pallet; PP, protractor muscle of pallet ; RP, retractor muscle of pallet ; RS, attachments of the siphons.

are clearly separate except distally, the margin of each cup covered with a yellowish-brown periostracum which is entire and separated from that of its neighbours, and drawn out into pointed processes laterally. The pallets are formed in special pockets of the mantle. The handle is first secreted and then the cone-in-cone units which are added as the animal grows. The distal one is the oldest while the younger and larger ones are added in a series. The shipworm fills its burrow and the soft outer surface secretes a calcareous tubing between the body and the walls of the burrow possibly as a protection against any noxious substance in the timber. This calcareous layer shows in X-ray photographs. The animal does not lie loose in the burrow for it is attached by means of the siphonal retractor muscles to the calcareous lining of the burrow at the posterior end. 1. The shell and mantle

The teredine shell (Fig. 5 ) is an irregular sub-globular structure composed of two valves each with a deep right-angled notch in the ventral half of the anterior margin. It is equivalve, each valve with a distinct anterior lobe and a posterior lobe called the auricle. The

352

N.

BALAKRISHNAN NAIR AND M. SARASWATHY

anterior lobe resembles a triangle which joins the median lobe by one of its long sides. The free angle of the lobe points forwards like a beak. At the dorsal free margin, the outline is interrupted by a deep sinus from which a smooth callus is reflected over its surface. The outer surface of this lobe is sculptured by fine ridges parallel with the ventral free margin, extending from the callus on the dorsal margin to the median lobe, where they meet almost at right angles those borne by the anterior region of this lobe. The denticulated ridges of the median lobe run parallel with the anterior free margin, bear stouter denticles and are more numerous than those on the anterior lobe. Some of the ridges in

FIG.5. Outer and inner views of the shell of a shipworm (Teredora). (1) anterior; (2) anterior median; (3) middle median; (4) posterior median; (5) auricle; (6) apophysis; (7) dorsal condyle ; (8) ventral oondyle ; (9) umbonal-ventral ridge.

the umbonal area appear worn by friction. The ridges are bent upwards and continued into the middle region where the ridges become smooth and low and extend into the posterior region where they finally cease. The middle region of the median lobe is further marked by a shallow groove running down from the umbonal region widening as it reaches the ventral margin, The posterior region of the middle lobe may be broad, thick and convex. Postero-dorsally it extends into the auricle (posterior lobe). The surface of the latter is marked by curved lines of growth which run parallel with its margin. This region of the shell is thin at the edges and slightly reflected outwards. When viewed from within, the middle lobe appears as a trough in which is lodged a part of the anterior region of the animal. The front edge of the posterior lobe forms a shelf projecting into the hollow of the median lobe. Towards the extreme ventral edge of this lobe, which is

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slightly bent inwards, appears a spherical knob-like thickening which forms a movable articulation with a knob borne by the opposite valve. This articulation is a feature peculiar to teredines and some pholads. Dorsally the margin of the middle lobe curves inwards forming a pronounced umbonal region, the tip or umbonal knob constituting a freely movable articulation with the similar process of the opposite valve. The elastic ligament is greatly reduced. The movement of the shell is around the axis formed by the umbonal knob and the ventral knob. The anterior and posterior adductor muscles can now oppose each other in action. Extending from the umbonal knob on the inner side of the shell is a broad sickle-shaped blade-like process, the apophysis, accommodated within the concavity of the middle lobe. This plate serves for the origin of the pedal retractor group of muscles. The shape of the larval shell of Teredo is that of a typical bivalve with equal convex valves nearly circular in outline. The valves are united by a well-developed hinge. After settlement and metamorphosis the pattern of growth along concentric lines changes to very unequal growth in different parts of the valves causing a transformation of the shell from the typical bivalve type. The condyles and the apophysis soon develop and the ventral edges of the valves grow faster than the remainder, causing them to gape before and behind. With the disappearance of the hinge apparatus and the development of additional articulation in the form of the condyles, the valves, instead of articulating at the hinge, begin to rock upon the knobs along a median transverse axis. The ventral edges of the valves grow faster than the rest of the shell causing the formation in the anterior edge of what soon becomes a right angle (Sigerfoos, 1908, Nair, 1956a). The median portion thus becomes the most prominent part of the shell. The posterior border also grows rapidly and flares outward so as to give better attachment for the posterior adductor muscle. A small portion of the dorsal anterior edge also flares outward, providing a face for the insertion of the anterior adductor muscle. The three layers, periostracum, prismatic layer and inner nacreous layer, though present, differ from those of other bivalves in being

FIQ. 6. Cross-section through posterior median area of the shell of Teredo navalia. (1) periostracum; (2) prismatic layer; (3) nacre. (After Miller, 1924.)

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1 2

3

Fra. 7. Section through the anterior median area of the shell of Teredo Itavnlis, cutting across the denticdated ridges. Abbreviations as in Fig. 6. (After Miller, 1924.)

relatively thickened and in the penetration of the prismatic layers by laminae of nacre (Figs. 6 and 7). Over the ridges the periostracum is thin. During boring, the suctorial foot is f?rmly attached to the wall of the burrow drawing the shell valves close to the blind, boring end of the burrow. The small anterior adductor muscle attached to the anterior edge of the shell valves just in front of the dorsal knob contracts first and this brings the anterior ends of the valves together spreading the posterior ends. The posterior adductor muscle is relatively much the larger and consists of homogenous coarse muscle strands, reddish in colour, attached to nearly the entire surface of the auricles of the shell. From their position of attachment and their size, it is evident that these muscles, instead of contracting simultaneously as in typical dimyarians, do so alternately drawing together the front and hind parts of the shell valves on the pivot formed by the dorsal and ventral knobs. This movement is responsible for boring. The large area of attachment of the posterior adductor indicates that the valves can be brought together more powerfully posteriorly than anteriorly. The divarication of the front ends of the shell causes the denticles on the outer surfaces of the shell valves to scrape against the wood with sufficient force to abrade it, the relatively feeble adduction through the contraction of the anterior adductor being sufficient t o bring the shell back to the normal position (Miller, 1924; Board, 1970). These boring movements are repeated, the animal rotating first in one direction and then in the other within the burrow. Since the animal feeds on the finely comminuted wood fragments, the shell valves can be considered as feeding as well as boring organs. Although in bivalve taxonomy, shell characters such as the shape of the valves, the hinge, ligament, sculpture, pallial line, periostracum and colour have all been extensively used, these have proved unsatisfactory in the classification of shipworms. Earlier workers like Bartsch (1922), Lamy (1927), May (1930), Moll and Roch (1931), Iredale et al. (1932), Roch (1940), Moll (1941, 1941a) and more recently Nair (1954, 1955a, 1959) have attempted specific determination on the basis of shell characters such as the shape and relative proportions of the different

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regions of the valves, the sculpture, hinge, condyles, apophyses, muscle scars, etc. Miller's work (1922) brought to light an amazingly wide range of variations in Teredo navalis involving practically every feature of the shell especially in the number of ridges, size and shape of the auricle, nature of denticles, etc. Nair (1959) illustrated a series of valves of Nototeredo norvagica from western Norway showing such variations (Fig. 8). Recent studies (Saraswathy and Nair, 1971) at Cochin on Nausitora hedleyi also showed the occurrence of similar variations especially in respect of the length/height ratio, number of ridges, length of the auricle, etc. With our present inadequate knowledge of the teredine shell it is too early to say how far shell characters may be employed satisfactorily for the determination of genera and species. In stray cases well developed shell characters may assist in identification when used in conjunction with the pallets as in Psiloteredo megotara (Hanley) and Xototeredo norvagica (Spengler) both living in the same habitat but having very similar pallets (see Nair, 1959). Three species of Bankia (Sigerfoos, 1908; Nair, 1955, 1957a; Bade, Masurekar and Bal, 1961) and one of Nuusitoru (Saraswathy and Nair, 1971) have been examined with regard to the structure of the mantle. This consists of two lobes which secrete the valves in a typical bivalve. I n shipworms the lobes have fused along their edges resulting in the formation of a long and delicate tube open in front for the protrusion of the foot and produced into long siphons posteriorly. The mantle is generally thin and translucent and not of uniform thickness. On the hind margins of the valves the mantle is raised up and extends over the umbonal region as a thickened muscular ridge. This duplication of the mantle, called the " cephalic hood " by Quatrefages (1849) was considered by him as the organ directly concerned with boring. Sigerfoos (1908) and Kofoid (1921) thought that it fitted into the burrow like a washer around the " head " preventing the fine particles of wood from entering the burrow. I n several specimens of Bankia indica examined the " cephalic hood " appeared very calloused suggesting frequent rubbing against the walls of the burrow. The epithelium of the hood in genera like Bankia and Nausitora projects on the median dorsal side behind the shell as a hump with a series of characteristic transverse foldings. The epithelial cells are tall and columnar containing granular cytoplasm. The rest of the mantle except the siphons is thin and the organs of the pallial cavity may be seen through it in fresh specimens. Since the entire surface of the mantle is capable of secreting calcium carbonate, the initial region of the burrow occupied longest by the animal normally receives the maximum limy deposition. Posterior to the shell valves on the dorsal and ventral surfaces the

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FIG.8. Teredo nmegica ( =Nototeredo norvagica). Top, shells showing variation in size and shape of the different regions ; bottom, pallets, illustrating variation in shape of the blade and stalk. (After Nair, 1959.)

mantle is often thick particularly in forms like Kuphus. I n Neoteredo, Bactronophorus and Nausitora, all mangrove or brackish water genera, the mantle is comparatively thicker than in other genera (Turner, 1966 ; Saraswathy and Nair, 1971). I n cross sections of the animal, the mantle on either side of the median line in Bankia indica and B . gouldi shows two prominent longitudinal thickenings. I n Nausitora hedleyi the

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mantle in the posterior region below the ctenidia reveals a greatly thickened median swelling (Saraswathy and Nair, 1971). The exact significance of these ridges which are absent in Teredo navalis and T . megotara (Purchon, 1941) is not clear. These folds probably form incomplete longitudinal partitions of the mantle chamber helping to some extent in regulating the movement of waste matter in the mantle cavity. The free edge of the mantle is thickened and consists of the outer, middle and inner folds typical of bivalves. Between the middle and the outer fold runs the periostracal groove. The middle lobe which is primarily sensory is devoid of any special sensory structures except at the tip of the siphons where sensory papillae occur. The outer fold and the periostracal groove are secretory, and so responsible for the ridges and denticles resulting in the growth of the shell by marginal increment. Periostracal fibres coalesce to form thick strands which pass over the edge of the shell. Within the connective tissue, especially of the anterior region of Naueitora hedleyi granular bodies appearing in serial sections have been shown to be developmental stages of certain parasitic protozoans, probably of Boveria as described by Ikeda and Ozaki (1918). Certain structures are associated with the connective tissue of the mantle. Hancock (1845) considered them t o be silicious particles responsible for the formation of the burrow. Deshayes (1848) observed non-nucleated mucous cells. Sigerfoos ( 1908) considered they were reserves of calcium used for the formation and thickening of the calcareous tube which lines the burrow. Nair (1957a) observed spherical nodular bodies in fresh connective tissue which were opaque in transmitted light and white in reflected light, soluble in water and turning russet when treated with iodine. Alcohol in which specimens had been preserved turned turbid. These structures were probably glycogen. Twarog (quoted by Turner, 1966)found that the " granules " in the mantle were insoluble in acid, in alkali and in distilled water and did not change colour when treated with iodine and so concluded the material was not glycogen. On prolonged heating a carbon residue was left suggesting that the substance is at least partially organic. The contradictory nature of these observations suggests that the structures examined were not all the same. I n the genus Kuphw the unusually thick mantle is composed of seven layers, an outer epithelium followed in order by thin layers of circular and longitudinal muscles, a thick layer of transverse muscles again by thin layers circular and longitudinal muscles and by the inner epithelium (Turner, 1966).

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N . BALAKRISHNAN NAIR AND M. SARASWATHY

Well defined ciliated tracts occur on the inner surface of the mantle. In Bankia gouldi Sigerfoos (1908) noted the presence of columnar and ciliated cells and, opposite the ends of the gills, he noticed that the mantle is lined with strongly ciliated cells with numerous mucous gland cells. A narrow strip of ciliated epithelium on the mantle opposite the branchial groove has been observed in Teredo navalis by Lazier (1924). Nair (1957a) noted in Bankia indica scattered groups of cilia on the inner mantle surface which posteriorly are arranged in two tracts which converge into a single tract behind the visceral mass. I n Teredo

FIG.9, Nausitora hedleyi. Section passing through the ciliated groove of the mantle showing the extra long cilia.

norvegica and T . megotara, Purchon (1941) recorded the presence of ciliated tracts on the mantle and scattered cilia on the visceral mass. I n Nausitora hedleyi, Saraswathy and Nair (1971) noticed two well defined tracts of cilia on the sides of the inner mantle epithelium extending parallel with the branchial groove. Though ciliated cells have been reported in the inner surface of the mantle in other shipworms they are neither so prominent nor arranged to form such well defined grooves. The unusual elongation of the branchial groove in N . hedleyi due to the great posterior displacement of the ctenidia probably necessitated the assistance of an additional band of strong, bristle-like cilia parallel with the branchial groove along the inner side of the mantle to propel

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the food rope towards the mouth. The ciliated groove in apposition with the branchial groove forms a ciliated tunnel. Posteriorly in the region of the ctenidia the grooves become shallow and eventually persist as two ciliated tracts. The cilia of these are unlike those in the groove in being scattered and short. These ciliary tracts could be traced to the very end of the mantle cavity. Further, the mantle epithelium along the roof of the epibranchial cavity is produced into a series of lamellae which project into the cavity especially dorsolaterally. There is greater development of muscle fibres along the roof of the epibranchial chamber and the epithelial lining is interspersed with gland cells. Nair (1957a) has recorded a concentration of mucous glands along the dorso-median line of the supra-branchial cavity and Sigerfoos (1908),noted a specialized type of gland in the posterior part but neither of these occurs in Nausitora hedleyi. A congregation of glandular structures has, however, been noted mid-dorsally at the beginning of the siphons in N . hedlleyi. 2. The adductor muscles The adductor muscles represent local enlargements and cross fusion of the pallid muscles (Yonge, 1953). The anterior adductor muscle is inserted on the ventral inner edge of the anterior lobe of each valve and the posterior adductor has its attachment on the inner face of the posterior wing of the shell-the auricle. Together they bring about a powerful rocking movement. The ability for alternate contraction of these muscles and the absence of the ligament help the shell valves to move on a dorso-ventral axis-and supply the shell with power for drilling. Pinkish in hue, they are composed of powerful strands of striated muscles. I n N . hedleyi the area occupied by the anterior adductor is only a tenth of that of the posterior adductor; both are approximately bean-shaped.

3. The pallets The pallets are unique structures characteristic of shipworms and show distinguishable differencesin the various genera. These variations are not only characteristic of the different species but also of individuals of the same species. I n shipworm taxonomy differences in the shape and proportions of the parts of the pallets have been regarded as important characters (seeBartsch, 1922,1923,1927,1927a;Iredale et al., 1932; Moll, 1941; Roch, 1940 ; Nair, 1954). I n many cases, the nature of the pallets alone has been considered as the basis of specific identification e.g. (Teredo (Teredo) beuufortanu Bartsch). I n some instances new species have been created on the basis of a single pair of pallets or a few

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BALAKRISHNAN NAIR AND M. SARASWATHY

of them (Bankia (Neobanlcia)barthelewi Bartsch). Lack of appreciation of the range of variations in the pallets has been responsible for the creation of a large number of species which later on turn out to be synonyms. Miller (1923) has shown that in San Francisco Bay the pallets of Teredo navalis exhibit a wide range of variations. Similarly Nair (1959) illustrated considerable variations in the size and shape of the pallets of Nototeredo norvagica from Western Norway. Apart from the genetic variations, the size and shape of the pallets may be considerably affected by age and wear and environmental factors. Drying up of the pallets and " exfoliation " of the periostracal cap are also likely to give an incorrect picture. Since these structures are constantly put to use to close the opening of the burrow they are subjected to considerable mechanical wear and tear. They are also chemically affected by the changes in the nature and composition of the ambient water. Variations in the nature of such deterioration can also take place in the pallets of living specimens. Those of Bankia (Nausitora) jamesi Bartsch have been illustrated by Turner (1966).Heavy settlement on a restricted substratum may misshapen the pallet in stenomorphic forms (gartsch, 192311;Nak, 1959). Even the two pieces of a single pair may be so unlike each other that they may be regarded as belonging t o different specimens. Therefore, in any taxonomic consideration at generic and specific levels based on differences exhibited by the pallets, the range of variations exhibited by them under different ecological conditions and due t o age and wear should be carefully considered before new species are described. The pallets of certain species such as those of Lyrodus exhibit remarkable variations (Fig. 10). This has led authors to create new species, most of which turn out to be ecological forms of the cosmopolitan, Lyrodus pedicellatus Quatrefages. The mechanism of the pallets in Bankia has been adequately described, and illustrated by Sigerfoos (1908). Turner (1966) has recently endeavoured t o trace the evolution of the pallet in the Teredinidae. According to her, during the evolution of the Teredinidae, following the development of the caecum and the separation of the intestine from the heart, a major divergence occurred. I n response to the need for an efficient mechanism to close the opening of the burrow one line accomplished this by adding new segments to the proximal end of the pallet giving rise to the segmented pallet line-the Bankiinae, and the other by depositing new material over the entire surface of the pallet leading to the non-segmented pallet line-the Teredininae. However, May (1929) interpreted this concentric incremental growth in Teredo navalis as fused segments. The evolution of the segmented pallet line is quite direct beginning with Nototeredo. The next step is

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FIU. 10. Lyrodua pedicallatua (Quatrefages). A series of pallets showing the nature of variations.

seen in the compact but more definitely segmented pallets of Spathoteredo and through Nazmitoru, the greatest specialization is reached in Bankia. The non-segmented pallet line apparently starts with a Teredora-

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like shipworm. Teredora and Uperotus are very closely related, with Uperotus probably the more primitive. Teredothyra, Bactronophorus, Neoteredo and Dicyathifer are related and all might have evolved from Teredora-like forms having simple pallets. Bactronophorus and Neoteredo are highly specialized and probably have not given rise to any other group. Some species of Teredo with single cupped pallets might have evolved from forms like Dicyathifer or from Psiloteredo and species with double cupped pallets probably stemmed from Teredothyra. Turner thus feels that Teredo as constituted by her is polyphyletic in origin evolved from Teredothyra, Dicyathifer and Teredora. Lyrodus represents the most highly evolved group in the non-segmented pallet line and has stemmed from Teredothyra. Information on the nature of growth of the pallet is helpful in many ways. It throws light on the nature of development of the different elements that compose this structure and may provide clues for evolutionary trends. It may assist in the correct identification of species since recent studies have shown that there may be noticeable changes in the shape of the pallet as a result of age. For example Rancurel (1955) has shown that the young pallets of Teredora malleolus (Turton) have double tubes and may easily be confused with those of species in Teredothyra and with Teredo fulleri Clapp. Close examination of the entire stages of development of the pallet in Teredora malleolus reveal the gradual broadening of the blade of the pallet and reduction of the diameter of the tubes consequent on the thickening of the base. The pallet of the adult specimens apparently does not show any sign of the double tubes. A similar condition has been illustrated by Turner (1966) in the same species from Bastia, Corsica. Again in Bankia carinata (Gray) Turner has shown that the young pallets are Lyrodus-like and could easily be confused with that genus. Monod’s studies (1952) on the pallets of Teredo (Psiloteredo) senegalensis Blainville have shown that petitii Recluz is just the juvenile stage and the ecotypical form of senegalensis. Certain growth stages of Teredo trulliformis Miller (Teredo clappi Bartsch) has been illustrated by Edmondson (1942). The young stages of this form resemble those of young fulleri. The growth of the pallets is influenced either by the addition of material over the entire surface and the extension of the blade laterally and distally, (Teredo, Psiloteredo, Neoteredo, Teredora, Dicyathifer and Kuphus) or by the addition of segments, the oldest being the smallest. New cones are slightly larger than the one that precedes giving rise to a plume-shaped pallet as in Bankia, Nausitora, Spathoteredo or Nototeredo. In these forms the stalk is continued to the very end of the blade, but growth takes place only at the proximal part of the pallet.

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In Teredothyra and Lyrodus massa the stalk extends only to the base of the inner element and is usually hollow (Turner,.1966). 4. T h e calcareous lining

The calcareous lining of the burrow varies in thickness and consistency. Their extremities (Fig. 11) may be single or paired and may protrude beyond the surface of the timber to protect the partially extended siphons (Turner, 1966), to prevent the entrance of foreign particles or predators between the mantle and the lining of the burrow (Roch, 1940), or as a reaction against the deposition of sediments over the surface of timber (Yonge, 1927). Such periostracal or calcareous collars have been recorded in Teredo navalis (Jefieys, 1860), Noto-

FIG.11. The details of the distal end of the calcareous tubing of the burrow of Teredo megotara (= Psiloteredo megotara) (m);and Teredo noruegica ( =Nototeredo norvagica) (n). (After Dons, 1946.)

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teredo norvagica (Yonge, 1927), Teredo utriculus (Roch, 1940), T . ( Teredothyra) dominicensis and T . sigerfoosi (Nototeredo knoxi) (Clapp, 1951). I n certain species with flattened pallets, e.g. Teredora and Nototeredo, calcareous transverse septa occur in the attenuated tips of the tubes. The pallets fit against these incomplete partitions, some distance within the aperture while closing the burrow (Dons, 1946). I n some species like Teredothyra dominicensis (Bartsch) the posterior

d

C

b

a

e

f

FIG.12. The distal ends of the siphons of shipworms : (a) inhalant siphon (slit open) of Teredo navalia; (b) exhalant siphon of Teredo utriculus; (c) inhalant siphon of Bankia minima; (d-g) sections passing through the inhalant siphons of: (d) T . navalis; (e) T . pedicellata; (f) T . utricuZus; (g) Bankia minima. (After Rooh, 1940) ; (h) posterior end of Nausitma fusticula showing the elaborate incurrent siphon ; (i) enlargement of a single " tentacle " showing the structure of the inner surface. (After Turner, 1966.)

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end of the tube may be partially or completely divided by a calcareous longitudinal partition, the inhalant and exhalant siphons each extending through a half of the partitioned tube (Turner, 1966). 5 . The siphons

The formation of siphons in the bivalves has been described by Yonge (1948) and those of shipworms are referable to the type B/C (Yonge, 1957). They have been described by Sigerfoos ( 1908) in Bankia gouldi, by Roch (1940) in Teredo utriculus, by Nair (1957a) in Bankia indica, by Bade et al. ( 1961) in Bankia minima, by Turner (1966) in Nausitora fusticula, Teredora malleolus and Bankia rochi and by Saraswathy and Nair ( 197 I ) in Nausitora hedleyi. Their appearance, whether united (except at the tip), partially separate or separate, in 34 species has been presented by Turner ( 1 966) who further suggested that siphonal characters such as length, extent to which they are separated, the number and size of the papillae and the colour and colour pattern, may prove useful in systematic work and might be of great assistance in the identification of species by the aid of the displayed siphons without disturbing the animal. That the characters of the siphons do exhibit distinguishable variations (Fig. 12) which may be of taxonomic value is evident from the observations of Roch (1940) on Mediterranean species and of Clapp ( 195 1 ) on Teredo sigerfoosi. Morton ( 1 970) finds specific differences between the siphons of T . navnlis and Lyrodu.3 pedicellatus. For detailed anatomical studies the work of Nair (1 957a) and Saraswathy and Nair ( I97 I ) should be consulted. 6 . The boring m~chonisir~ The ability to bore into hard substrata is a habit which has evolved independently i n no less than seven super families of the Bivalvia. In the Adesmacea this ability appears t o have been derived from the primitive infaunal burrowing habit by adaptation to deep burrowing in stiffer and stiffer substrates until true boring was developed. In all other groups, with the exception of Platyodon, the sole boring genus of the superfamily Myacea, true boring probably developed as a further specialization of an epifaunal, byssally-attached existence on rock and especially of the habit of nestling in crevices (Yonge, 1963). The structural modifications of the basic bivalve form associated with the boring habit liiive beeti extensively studied (Miller, I924 ; Yurchon, 1955). All the niembers of' the Adestnucea show considerable modificatioti t o boring, but those of t h e Pholadidae which bore into rock and other solid substrates including peat, sandstone, limestone, shale and mudstone are less specialized than members of the X ylophaginidne

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(Purchon, 1941) and Teredinidae which bore into wood. The earlier theories concerning the method of boring have been summarized by Miller (1924) whose detailed observations on Teredo established that in this species the shell is the only tool used in boring, the foot and cephalic hood serving to hold the animal in position in the burrow while the shell is moved by the muscles attached to it. Recently Board (1970) investigated the tunnelling operations of shipworms using the technique of radiography and made certain interesting observations. He noted that the boring end of the burrow contains water which the shipworm removes by forcing it into the grain at the unlined portion of the wood ahead of it ; and the lubrication of the shell valves is accomplished by small, shrinking movements of the animal within the burrow. Although many authors have described the boring action, descriptions vary widely in scope and differ in interpretation of the events involved. For example most authors agree that during boring the animal rotates, but Yonge (1963) attributes this rotation to the attaching foot moving first in one direction, then in the other while Morton (1964) considers that rotation in all the Adesmacea is caused by asymmetrical action of the adductors, the shell turning up to 90' alternately in each direction. It is generally accepted that in all Adesmacea the boring action is purely mechanical, but the exact mechanisms involved have not been clearly explained. According to Lane and Tierney (1951) the denticulated shell-valves maintain contact with the advancing face of the burrow with the aid of turgor developed in the mantle cavity. This intramantle pressure in Teredo pedicellata is of the order of 5-17 mm water. I n these long, flaccid bivalves it is this internal mechanism that insures effective apposition of the boring tools with the blind, boring end of the burrow. The production and maintenance of turgor is the result of the interaction of siphonal musculature, gill cilia and the mantle. Nair and Ansell (1968) have described the main activities during boring by Zirphaea crispata using techniques similar to those which have been applied to the study of the burrowing action and fluid dynamics of bivalves (Hoggarth and Trueman, 1967 ; Trueman, 1966, 1967 ; Ansell and Trueman, 1967). I n the Teredinidae a new type of movement about a dorso-ventral axis has been perfected and the shell valves have become greatly specialized as a boring instrument free from attachment of the siphonal muscles. The adaptational sequence (Fig. 13) involved in this change in function of the adductor muscles in the Adesmacea has been followed out by Nair and Ansell (1968). Recent observations of Ansell and Nair (1969) have shown that wood boring may be achieved by the same movements as those involved in rock boring, but may also in some species involve

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further elaboration of the basic cycle. I n Martesia similar movements are employed in wood boring to those used by Zirphaea in boring into clay or soft rocks. I n this genus no further specializations are involved. The boring cycle of Xylophaga dorsalis, on the other hand, represents a further elaboration by the replications of the contractions of the adductor muscles, thus showing greater development of that part of the cycle which represents the application of effective abrasive action. The climax of specialization is reached in the Teredinidae where the adductor muscles antagonize each other directly across the fulcrum formed by the dorsal and ventral articulations. The antagonism between the adductor muscles and siphonal retractor muscles noticed in forms like A

B

C

I FIG.13. Diagram illustrating the main line of evolution of the rock- and wood-boring habits of the Adesmacea from burrowing. A, Mercemria mwcenaria representative of shallow burrowing form ; B, M y a arenaria representative of a deep burrowing form ; C, Zirphaea crispata representative of a rock-boring pholad ; D, Xylophaga dorsalis the wood-boring pholad and E, Teredo navalis the wood-boring teredinid. (After Nair and Ansell, 1968.)

Zirphaea crispata is probably no longer important owing to the unique backward extension of the body and the consequent displacement of the siphons far from the posterior margins of the valves. Accounts of the boring mechanism of members of the Teredinidae suggest that there also replication of rocking abrasive movements occurs (Miller, 1924 ; Turner, 1966). Specialization of the shell in shipworms has proceeded 80 far that it has almost lost its protective significance and remainn only as a drilling tool par excellence.

7. The digestive system Deshayes (1848) and Beuk (1899) were two early workers to study this system. Sigerfoos (1908) briefly described the alimentary canal in Bankia gouldi. Lazier (1924) and Nair (1957a) dealt with the system in

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considerable anatomical detail in Teredo navalis and B a n k indica respectively. The structure and function of the digestive diverticula of Teredo were described by Potts (1923) and in greater detail by Yonge (1926). Purchon (1941) studied the labial palps and ciliary mechanisms in Teredo norvegica and Teredo megotara. The same author (Purchon, 1960) has also given excellent accounts of the stomach in two species of shipworms, Psiloteredo amboinensis and Teredo manni. Bade et al. R

MG

I

APP

VG

I

I

I

MG

II

I

GO

I ?,

DD BP

CTI

tv!G

G

ES IS

FIG.14. Teredofurcijeru. General disposition of the organs of the mantle cavity as seen from the right side (semi-diagrammatic sketch). AA, anterior adductor muscle ; AC, anal canal ; AN, anus ; APP, caecum ; AU, auricle ; BP, brood pouch ; CTI, coiled typhlosole of the intestine ; DD, digestive diverticula; ES, exhalant siphon ; F, foot ; G, gill ; GO, gonad ; IS, inhalant siphon ; K, kidney ; M, mouth ; MG, midgut ; 0, oesophagus ; PA, posterior adductor muscle ;PC, pericardium; R, rectum ; SS, style sac ; ST, stomach ; V, ventricle ; VG, visceral ganglion.

(1963-64) have described this system in Bankia minima. Saraswathy and Nair (1971) have recently studied the gut in Nausitora hedleyi, Teredo furcifera and Teredora princesae. The general layout of the system in a number of species has been described with the aid of careful dissections by Turner (1966). Morton (1970) has recently given a most detailed account of the structure and functioning of the stomach in Teredo navalis and Lyrodus pedicellatus. While the general disposition of the alimentary canal (Fig. 14) is similar in forms like Teredo navalis Linnaeus, T . bartschi Clapp, T . furcifera Von Martens, Lyrodus pedicellatus (Quatrefages), Bankia

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gouldi (Bartsch), B. setacea (Tryon) and B. carinata (Gray), variations exist in different genera. While the labial palps are free and distinguishable in Teredora princesae, T . malleolus, Uperotus clavus, U.rehderi, Psiloteredo megotara, Nototeredo norvagica, N . knoxi and N . edax, they are attached and inconspicuous in Kuphus polythalamia, Bactronophorus thoracites, Neoteredo reynei, Dicyathifer manni, Teredothyra matocotana, T . dominicensis, Psiloteredo healdi, P. senegalensis, Teredo furcifera, T . fulleri, T . clappi, T . navalis, T . poculifer, Lyrodus massa, L. pedicellatus, L. takanoshimensis, L. mediolobata, Spathoteredo spatha, X. obtusa, Nausitora fusticula, N . hedleyi, N . dunlopei, Bankia gouldi, B. indica, B. australis, B. setacea and B. campanellata. Though shipworms have the basic palp structure of an outer and inner pair, these structures vary considerably in size and efficiency. In all species hitherto studied the outer and inner palps may be recognized. Variations in the relative proportions of these are to be attributed to habitat specializations and to the degree of dependence on planktonic food. The palps of Teredo norvegica (Nototeredo norvagica) are by far the most conspicuous and perhaps capable of quantitative selection (Purchon, 1941). That the nature of the palps in the Teredinidae has an evolutionary significance is evident because all the genera known to possess free and distinct labial palps are comparatively less evolved than those genera with reduced palps. A trend towards reduction in functional efficiency is evident during the course of evolution where a noticeable shift from dominant plankton feeding towards dominant cellulose feeding has taken place with associated adjustments in structure and physiology. I n the digestive system, the organs which show noticeable variations are the stomach, caecum and intestine. Moreover, the anal canal may be open or closed. The stomach is globular in genera such as KzLphus, Bactronophorus, Neoteredo, Dicyathifer, Teredothyra, Uperotus, Psiloteredo and Nototeredo ; is elongate-globular in Teredora and elongate in Teredo, Lyrodus, Nausitora and Bankia. Five evaginations of the stomach have been reported for Teredo navalis, Bankia indica and Nausitora hedleyi. These are the style sac, the lateral pouch (=left pouch of Purchon, 1960), the dorsal caecum (=dorsal hood of Purchon), the digestive diverticula and the caecum (=appendix of Purchon). The stomach in the above is assignable to type V (Purchon 1960). By far the most conspicuous part of the gut is the caecum (appendix) which extends horizontally backwards. It is absent in the genus Kuphus, is small in Dicyathifer, Teredothyra matocotana and Nototeredo knoxi, moderately large in Bactronophorus, Teredothyra dominieensis,

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Teredora, Uperotus, Psiloteredo, Teredo, Lyrodus, Nototeredo edax, Xpathoteredo, Nausitora fusticula and Bankia and large in Nausitora hedleyi and N . dunlopei. In Teredora and Uperotus, it is doubled on itself to the right. Except for minor differences, the appendices of Bankia gouldi, B. setacea, B . indica and Nausitora hedleyi are similar in general structure and histology. The typhlosole in this organ varies in size and extent and in the nature of coiling. In species described by Deshayes (1848) the caecum is reported as thin-walled with a narrow orifice and with a typhlosole (" valvule ") like a funnel and the organ doubling on itself to end blindly. It is further reported that the intestine takes off from it. The description given by Quatrefages (1849) is

FIG.15. Teredora princesae. General disposition of the organs of the mantle cavity of the anterior part of the body as seen from the right side. Note the caecum which is doubled on itself to the right in this species. Lettering as in Fig. 14.

essentially the same but he denies that the intestine leaves the caecum. In Psiloteredo amboinensis, Purchon (1960)describes a caecum which is strikingly different in many respects from those in other shipworms. I n this species a large fleshy typhlosole hangs inside the full extent of the caecum. Further, the roof bears a longitudinal band which is transversely striated. This bears cilia which beat from the centre towards the lateral margins. This wood sorting caecum is homologous with the postero-dorsal caecum of the Tellinacea (Yonge, 1949) and occurs in all families of the Adesmacea (Purchon 1960). Purchon (1955) has shown that the caecum of the Pholadidae is comparable to the wood sorting caecum of Xylophuga and Teredo. Based on the structural and functional similarity of the postero-dorsal caecum of the Tellinacea and the

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THE BIOLOGY OF WOOD-BORING TEREDINID MOLLUSCS

caecum of the Adesmacea, Purchon (1955) concludes that these are homologous and provide reliable evidence of relationship. The bent caecum of Teredora (Fig. 15) and Uperotw is probably associated with the need for the storage of wood fragments since in these genera the elaborate typhlosole is not present. A rudiment of the typhlosole is evident in the caecum of Teredora princesae. I n Nototeredo norvagica a typhlosole is apparently absent. I n Neoteredo the caecum is of moderate size. Species having large caeca occur in the highly specialized genus Nausitora where this organ is noteworthy not only for its size but also for its contained greatly coiled typhlosole. Similarly in both the advanced genera Bankia and Teredo the caecum is large with a doubly coiled typhlosole. Thus this organ seems to be an index of specialization. The larger and more specialized the appendix, the higher its place in the evolutionary scale. Nevertheless, the reasons for the development of an elaborate typhlosole which is obviously a device for increasing the area of absorption within the caecum is difficult to understand in the context of the present concept of the function of the caecum as an organ merely for the temporary storage of wood fragments. However, in the light of the recent emphasis on the role of bacteria and fungi in the digestive process of wood-boring bivalves it is possible that‘the digestion of at least a part of the wood occurs within the caecum. It is not clear how the wood stored in the caecum finds its way into the stomach and then into the tubules of the digestive diverticula. The wall of the caecum does not appear sufEciently muscular t o force the contents out and it is difficult to understand the method by which the stored fragments emerge. Purchon suggests (quoted by Reid 1966) that “ the stored particles may be flushed out by the closure of the midgut entrance and the contraction of the stomach.” According to Reid (1965), by their contraction the adductor muscles expel the contents of the caecum as a mucus bound mass. It is possible that the movements of the animal within the burrow also play an effective role in this process. There is an apparent relationship between the elaboration of the cwcum and reduction of the labial palp. For example : (1) the simple caecum without the coiled typhlosole of Nototeredo norvagica and its large palps capable of selective sorting of food materials ; (2) the large caeca of Nausitora, Teredo and Banlcia and their inconspicuous palps incapable of quantitative selection. Since the terms “ liver ” or “ hepatopancreas ” imply an assumption regarding their homology and since they are digestive in function, the mass of tubules round the stomach are known as digestive A.M.B.-9

13

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N. BALAKRISHNAN NAIR AND AT. SARASWATIIY

FIG.16. Bankia indica ( = B . carinata). (a)Transverse section through a part of the digestive diverticula ; (b) Transverse section through a part of the specialized region of the digestive diverticula.

diverticula (Yonge, 1926). Sigerfoos (1908), Lazier (1924) and Morton (1970) described them while Potts (1923), Yonge (1926) and Morton (1970) discussed their functions. Details of their distribution in

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Bankia indica, Nausitora hedleyi, Teredofurcifera and Teredora gregoreyli (= Teredora princesae) are given by Nair (1957a), and Saraswathy and Nair (1971). The diverticula (Fig. 16) are distinguishable histologically into two portions, the so-called “unspecializedregion ” composed of thick walled columnar cells forming the tubules considered by Potts (1923) as excretory and the “ specialized ” diverticula consisting of thin walled wide tubules which are specially concerned with the reception and intracellular digestion of wood. The lumen of the former is not of uniform diameter and in cross sections they appear cruciform or triradiate. The

FIG. 16(c). Transverse section through a part of the digestive diverticula to show the difference hetween the specialized and unspecialized regions of the digestivediverticula in Nuusitom hedleyi.

functionally different types of diverticula have been reported in several species (Sigerfoos, 1908 ; Potts, 1923 ; Yonge, 1926 ; Nair, 1957a ; Saraswathy and Nair, 1971) but in Teredoprincesue the distinction between specialized and unspecialized regions is not evident. The disposition of the digestive diverticula too seems to vary in different species. In Bankia indica (Nair, 1957a), the diverticula are distinguishable into three groups according to their distribution around the stomach. Most of the anterior diverticula occupy the interior of the foot forming a system of blind tubules opening in%othe anterior part of the stomach by a number of openings on the right wall and by a single large opening in the anterior wall of the lateral pouch. Below the stomach, closely applied to its wall and opening into it by four orifices

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N. BALAKRISHNAN NAIR AND M. SARASWATHY

lies the second group, The posterior and by far the largest mass is distinguishable into a large more dorsal right half and a small left half. The former is brownish green and lies on the right side of the posterior part of the stomach while the latter is fawn-coloured and composed of few tubules containing particles of wood, a condition similar to what Lazier (1924) found in Teredo navulis. The condition in Nuusitoru hedleyi (Saraswathy and Nair, 1971) is slightly different. The set of tubules forming the ventral " liver " noticed in Teredo (Lazier, Zoc. cit.) and Bunkiu (Nair, 1957a) is not distinguishable in Nuusitoru hedleyi. The major part of the diverticula forms a large, compact mass closely attached to the stomach and the anterior part of the caecum. Here, the diverticula are disposed chiefly in the lateral and ventral regions of the stomach. The whole mass shows a characteristic appearance with a comparatively small, deeply pigmented region on the right side which represents the region of the unspecialized part of the digestive diverticula. The relative proportions of the two regions are also different. I n Nazcsitora hedleyi there is a pronounced development of the lightly pigmented specialized region compared with the unspecialized part which is represented only as a small mass on the right side. The main passages through which the specialized digestive diverticula bommunicate with the stomach are apparently devoid of any special device aiding in the selection, acceptance or rejection of material. However, Potts (1923) noticed in fresh material of Teredo that the cells of the tubules of the specialized region carry long, easily retractile cilia which beat with a languid motion. Probably particles of wood from the stomach and caecum are drawn into these diverticula partly through the movements of the anterior part of the body while boring. The ducts of the unspecialized region of the digestive diverticula are lined by tall, columnar, ciliated cells with centrally placed nuclei. Yonge (1926) has shown that the digestive diverticula are not secretory. Nair (1957s) has observed the occurrence of amoeboid cells ingesting wood fragments in the specializedpart of the digestive diverticula. A correlation between the development of the specialized part of the digestive diverticula and the elaboration of the caecum (=appendix) is also evident in the Teredinidae. I n Teredoru and Nototeredo where the caecum is less developed the specialized part is absent while in Nuusitoru where the caecum is most fully developed the specialized part of the digestive diverticula is proportionately large. However, the apparent relationship between the development of the specialized digestive diverticula and the ability to digest cellulose has yet to be clearly established.

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I n respect of the intestine, shipworms are of two types: (1) those in which this takes a forward course into the foot where it loops over the style-sac; and (2) those in which it does not loop over the style-sac. Bactronophorus, Neoteredo, Dicyathifer, Teredothyra, Teredora, Uperobus, Psiloteredo, Nototeredo norvagica and N . knoxi are in the former category while Teredo, Lyrodws, Nototeredo edax, Spathoteredo, Nausitora and Bankia are in the latter.

FIG.17. Bankia indica. ( = B .carinata). The coiled typhlosole of the intestine.

A longer and coiled mid-gut is characteristic of less specialized shipworms. The length of the mid-gut also varies considerably in different genera. Nototeredo norvagica has a highly coiled mid-gut. I n species of Teredora and Psiloteredo the gut characteristically loops over the style-sac. In Teredo, Bankia and Nawsitora, She mid-gut makes a sharp backward turn beyond the dilated portion containing the coiled typhlosole of the intestine and so is comparatively short. At the beginning of the mid-gut in certain shipworms (Bankia,

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N . BALAKRISHNAN NAIR AND M. SARASWATHY

Teredo and Nausitora) there is a conspicuous bulbular portion containing within it a highly coiled typhlosole (Fig. 17). This is absent in Teredora princesae. According to Purchon (1960) it probably serves as a valve preventing the passage of undigested particles of wood from the appendix into the mid-gut, adding that the tension that would develop on the stomach wall when the stomach and appendix are filled would force some of the stomach contents into the mid-gut. I n such instances this typhlosole probably acts like a stopper preventing the entry of stomach contents into the narrow part of the mid-gut. The anal canal is closed in Bactronophorus, Neoteredo, Dicyathifer, and Teredothyra and is open in all other genera of timber boring Teredinidae (see Turner, 1966). 8. The ctenidia The ctenidia of shipworms are considerably reduced (Fig. 18). According to Turner (1966) they are represented by the inner demibranch only but a vestige of the outer demibranch is found in some species. Ridewood (1903), Atkins (1937) and Morton (1958) also consider this single demibranch as the inner one though Purchon (1939) thinks it to be the outer demibranch in both Xylophaga and Teredo. Each ctenidium consists of homorhabdic branchial filaments inserted uniformly on a vascular axis of connective tissue traversed by muscle fibres. The interfilamentar junctions are organic indicating a synaptorhabdic condition and the intrafilamentar junctions are vascular representing a typical eulamellibranch condition. The nature and extent of the ctenidia vary considerably in different genera. For example in Teredora and Uperotus the ribbon-like ctenidia extend from the base of the siphons to the labial palps with a well-developed marginal groove. I n others the ctenidia are much smaller, consisting of an anterior section of a few ascending filaments (five in Teredo navalis, seven in Teredo megotara, eight in Nausitora hedleyi, nine in Bankia indica and ten in Banlcia minima and in Teredo norvegica) separated from the major part of the ctenidium situated behind the visceral mass. The two sections are connected by a branchial groove passing along the dorso-lateral side of the caecum. I n Banlcia gouldi Sigerfoos (1908) considers this groove as formed by the great broadening of the 10th or 11th filament during post-larval development. When compared to the ctenidia of other shipworms, those of the adult Nausitora hedleyi are comparatively short and the posterior section lies far back in the mantle cavity away from the caecum in full grown specimens. The progressive displacement of the ctenidia in Nausitora hedleyi during the growth in length of the body is shown in Fig. 19. In transverse sections through

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FIG.18. Figures illustrating the disposition of the organs in the mantle cavity especially the ctenidia of three representative genera of shipworms. A, Teredora princesue with the ctenidia extending from the side of the mouth to the siphons ; B, Teredo fweifera representing the typical condition in shipworms and C, Nmaitora hedleyi with reduced ctenidia. AA, anterior adductor muscle ; AC, anal canal ; AN, anus ; APP,caecum; ARD,afferent renal duct ;AU, auricle ;BP, brood pouch ;CO,collar ; CTI, coiled typhlosole of the intestine ; DD, digestive diverticula ; EC, epibranchial (exhalent) cavity; ERD, efferent renal duct; ES, exhalant siphon; F, foot; G , gill; GO, gonad; IS, inhalant siphon; K, kidney; M, mouth; MA, manble; MG,midgut ; 0,oesophagus; PA,posterior adductor ; PC, pericmdium ; R, rectum ; RD, renal duct ; SDD, specialized part of the digestive diverticula ; SS, style sac ; ST,stomach ; TA,typhlosole of the caecum ; V, ventricle ; VG, visceral ganglion.

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N . BALAKRISHNAN NAIR AND M. SARASW-ATHY CO

EC

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FIG.19. A series of three specimens of Nauitora hedleyi of different growth stages to show the displacement of the organs in the mantle cavity during the growth in length of the animal. A, Specimen 0.3 cm in length; B, specimen 2.2 cm long and C, specimen 16.5 cm long. AA, anterior adductor ; AC, anal canal ; APP, caecum : AU, auricle ; CH, cephalic hood ; CO, collar ; DD, digestive diverticula ; EC, epibranchial (exhalant) cavity ;ES, exhalant siphon ; F, foot ; G, gill ; GO, gonad : IS, inhalant siphon ; K, kidney ;M, mouth ;MC, mantle cavity ;MG, midgut ;R, rectum ; SDD, speoialized region of the digestive diverticula ; V, ventricle ; VG, visceral ganglion.

the body the ctenidia are seen to occupy only a small portion of the dorsal part of the branchial chamber. Based on the position of the afferent branchial vein in the ctenidial axis, Purchon (1941) believes the filaments of the anterior part to be the ascending gill lamellae and the descending gill lamellae to be represented by the inner wall of the branchial groove. The ctenidial axes of the right and left demibranchs converge behind the caecum into a single common dorso-median axis bearing the filaments of the demibranch of the two sides. Examination of the sections through the gill across the axis brings out the differences in the shape of the demibranchs in the different species (Fig. 20). I n Bankia indica the descending limb of the lamellae of the demibranchs pass first laterally and then downwards (Nair, 1957) ; in Teredo nawalis, the direct lamellae descend, but the reflected lamellae pass horizontally inward and unite with one another in the

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FIG. 20. The gills of shipworms. Sections of shipworms taken towards the posterior part of the body beyond the caecum through the gills (ctenidia). Note the nature and extent of the gills in the different genera. ( 1 ) Bankia go&; (after Sigerfoos, 1908); (2) B.ircdica (after Nair, 1965); (3) Teredo navalis (after Ridewood, 1903); (4) Nausitora hedleyi (after Saraswathy and Nair, 1971); (5) Psredoficrcifera (after Saraswathy and Nair, 1971); (6) Teredora princesae (after Saraswathy and Nair 1971). AAF, Ascending arm of filament; ABV, afferent branchial vein; ARV, afferent renal vein ; CABV, common afferent branchial vein; CMT, ciliated mantle tract; DAF, descendmg arm of filament; EBV, efferent branchial vein; EC, epibranchid (exhalant) cavity ; G, gill ; GC, gland cells; GDS, glands of Deshayes ; IBC, infra-branchial (exhalant) cavity ; ILJ, interlamellar junction; MA, mantle ; MG, mantle groove; MGR, branchial or food groove; PAR, pallial artery; PAS, stalk of the pallet.

median line (Ridewood, 1903). The shape and length of the gills in several species have been described by Turner (1966). I n Bactronophorus the descending limb of each lamella is nearly straight while the ascending limb extends laterally before bending upward forming a U-shaped lamella. I n Neoteredo the broad and flat gills form little more

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I?. BALAKRISHNAN NAIR AND M. SARASWATHY

than a septum between the inhalant and exhalant chambers (Turner, 1966). The descending lamellae extend almost horizontally in Teredo norvegica instead of downwards as in Bankia gouldi (Sigerfoos, 1908) and in Teredo megotara (Purchon, 1941). I n Nausitora hedleyi, conditions are generally similar to those in Teredo megotara even though the descending lamellae pass outwards. The marginal groove, though reported in all species studied in detail, varies. In some it is deep and well defined, in others like Nausitora hedleyi it is very shallow and too insignificant to appear in transverse sections. I n Xylophaga also the ctenidium possesses no marginal groove (Purchon, 1941). Each branchial filament has the usual three kinds of cilia, frontals, latero-frontals and laterals (Fig. 21). The ctenidia vary greatly structurally and in functional eficiency. I n bivalves the ctenidia are not only organs of respiration but are also FC

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FI IFJ

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FIG. 21. A, Section through the gill laminae showing the ciliation of the filaments, position and structure of the glands of Deshayes in Bankia indica ( =B. carinata); B, section of the descending lamella of Teredo navalis (after Ridewood, 1903). AFC, abfrontal ciliated cells; CHR, chitinous supporting rod; FC, frontal cilia ; FI, filament; GDS, glands of Deshayes; IFJ, interfilamentar junction; ILS, interlamellar space ; LC, lateral cilia ; LFC, latero-frontal cilia.

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concerned with plankton feeding. I n the Teredinidae consequent on a shift in emphasis from plankton feeding to a diet consisting chiefly of wood fragments, the ctenidia have undergone relative changes. I n two genera, Teredora and Uperotus, the ctenidia extend the entire length of the animal from the base of the siphons to the mouth (Saraswathy and Nair, 1965). Others have discontinuous ctenidia. I n Nausitora hedleyi, N . dunlopei and Neoteredo reynei, the ctenidia are short with rather truncate lamellae, an extreme case of reduction in contrast to the condition in the genera Uperotw and Teredora. The condition in others seems to be intermediate between these extremes. This apparent differencein the extent and efficiencyof the ckenidium is interestingly correlated with the extent of the development of the apecialized region of the digestive diverticula which probably represents the region for the reception and intracellular digestion of,wood particles. I n Teredora princesae where the ctenidia are well developed with the most extensive gills bearing long gill lamellae, the specialized part of the digestive diverticula cannot be seen even in serial sections. Probably, this species feeds almost entirely on plankton. I n Teredo furcifera where the ctenidia are of medium size, the specialized part is distinguishable histologically while in Nausitora hedleyi where the ctenidia are considerably reduced in extent the specialized region forms the dominant part of the digestive diverticula. Nawitora fusticula is interesting in that it bears short truncate gills and apparently has secondarily returned to filter feeding by adding the filtering mechanism (Fig. 12, h) to the end of the inhalant siphon (Turner, 1966). I n all cases, however, the ctenidia must assist in feeding by the collection of the small amounts of nannoplankton needed to supplement the scarce nitrogenous constituents present in the wood. Morton (1970), who describes the various cilary currents in Teredo nacalis and Lyrodus pedicellatus, finds little evidence of selection. Both wood particles and plankton enter the mouth. 9. Glands of Deshayes

These organs are peculiar to shipworms. Sigerfoos (1908) who named them described them in different degrees of development in Teredo dilatata, Bankia gouldi and Teredo navalis and distinguished three groups, one investing the gill lamellae, another in the tissue beneath the umbonal region of the shell and the third inside the afferent branchial vein. Deshayes (1848) had considered that these were separate structures with different functions. The first group occur packed within the interfilamentar spaces of

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N. BALAKRISHNAN NAIR AND M. SARASWATHY

the gill especially around the gill axis (Fig. 21). In Bankia gouldi, Sigerfoos distinguished between spherical bodies and structures derived from ramifying dentritic processes. Enlarged portions of the dentritic processes may become surrounded by specialized epithelial cells derived from those lining the gill or these cells may enclose a granular protoplasm with lightly staining nuclei and darkly staining rods projecting towards blood spaces inside the gills. I n Bankia indica, Nair (1957a) recognized in the gill laminae two structures composed of cells differing in histological details. A highly irregular ramification of filamentous

FIU. 22. Nausitora hedleyi. Section through the ctenidium showing the glands of Deshayes. ( x 75.)

structures lie in the epithelial walls of the gill laminae. They contain numerous deeply staining nuclei strewn indiscriminately in a mesh of granular cytoplasm without cell boundaries. The second type differs markedly being composed of spherical bodies which take a deep stain with Delafield’s haematoxylin. The spherical bodies occur in groups of two, three or four and are distributed irregularly in the internal spaces of the gill lamina. I n Bankia indica these glandular structures occur only in the gills. The umbonal portion of the gland found in Teredo dilatata and Bankia gouldi is absent. From these glands on either side a narrow cylindrical duct passes forwards by the side of the branchial groove, its lumen containing granular cells which stain deeply and open on either side of the mouth. The arrangement of the different cellular

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elements of the glands and their disposition in the gill differ considerably in B a n k i a indica and B. qouldi. Saraswathy and Nair (1971) have described the glands within the interlamellar spaces in the gill of Nausitora hedleyi (Fig. 22). These are groups of rounded bodies which appear as single units or more commonly in groups within the body of the gill. Each seems to be made up of several closely packed spherules and each spherule in turn contains a granular substance. Identical structures are also seen lying loose within the ducts of Deshayes running

FIG.23. Nausitora hedleyi. Section through the duct of Deshayes in the afferent branchial vein. ( x 301.)

within the afferent branchial veins which run parallel to the epibranchial canals. These ducts are in free communication with the glands lodged within the gill. I n Teredo furcifera the ducts are continued towards the very anterior end where they bent towards the middle to open into the anterior part of the oesophagus. Sigerfoos (1908) states " From the first, there is close association between the gland and the gill." As the latter grows, the filaments become invaded by the gland and as the anterior ten filaments become separated from the rest of the gill, the two parts of the gland thus differentiated remain connected by a long, narrow duct which accompanies the epibranchial canal and lies in the afferent branchial veins. With the separation of the two parts of the gill the intervening part of the gland disappears

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N. BALAKRISHNAN NAIR AND 31. SARASWATIIY

in Bankia gouldi and Teredo navalis but persists in Teredo dilatata. Sigerfoos also noted a duct leading to the exterior and opening at the side of the mouth on the ventral side of the velum in the larvae. The opening of the duct into the oesophagus in Teredo furcifera suggests several possibilities concerning the function of this gland. Whether these glands have any role in the digestion of cellulose has to be ascertained on the basis of histochemical and physiological tests. I n Teredora princesae the umbonal portion of this gland is well developed (Saraswathy and Nair, 1971). That part of the gland in the gill laminae, especially around the gill axis, in N . hedleyi, B. gouldi and B. indica is apparently not represented. The ducts of Deshayes in the afferent branchial vein (Fig. 23) contain a special development of this gland with minute filamentous structures and also a few well defined rounded bodies containing granular material. Probably this represents the glandular part reported by Deshayes within the afferent branchial veins. Anteriorly beneath the umbo there is a massive development of this organ which is continuous with the portion contained within the afferent branchial veins. This shows that all are essentially parts of the same structure as suggested by Sigerfoos. Deshayes considered that the secretion from umbonal glands softened the wood and that those in the gill served as a source of nourishment for the viviparous embryos. The function of these peculiar structures unique in the Teredinidae is unknown. Whether they are concerned with the elaboration of some internal secretion for whose formation the presence of both blood and water is necessary as suggested by Sigerfoos, though reasonable, remains to be investigated. The nutritive function suggested by Deshayes is not convincing since they are present in oviparous species such as Banlcia gouldi, B. indica and Nausitora hedleyi. 10. Circulatory system Menegaux (1890) described the circulatory system in Teredo navalis

Sellius (Linne), T . norvegica Spengler and T . pedicellata Quatrefages. The first adequate account was given by Sigerfoos (1908) for both the young and adult Banlciagouldi,even though as early as 1684, Redi noted the possession of a heart which is discernible with the naked eye in shipworms. Sigerfoos observed the same fundamental plan in the three species B. gouldi, T . navalis and T . dilatata, though in the last named, because of the more posterior position of the gills, the heart-especially the aorta-like part of the ventricle-is more elongated. The heart lies in a tubular pericardium on the apparently dorsal, but morphologically ventral side of the intestine. It varies considerably

THE BIOLOGY OF WOOD-BORING TEREDINID MOLLUSCS

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in size and position, in the form of the ventricle and in the length of the auricles. It may be placed ( 1 ) towards the anterior end of the body as in such genera as Bactronophorus, Neoteredo, Dicyathifer, Teredothyra, Teredora, Uperotus, Psiloteredo and also in species like Teredo fulleri, Lyrodus pedicellatus, L. takanoshimensis, L. mediolobata, Bankia gouldi, B. australis, B. setacea and B. campanellata; (2) in a median position as in Kuphus polythalamia, Teredo furcifera, T . clappi, T . navalis, T . pculifer, Lyrodus massa, Nototeredo norvagica, N . knoxi, N . edax, Spathoteredo spatha and S. obtusa; or (3) posteriorly as in Nausitora fusticula, N . hedleyi and N . dunlopei. The length of the heart in relation to the total length of the animal dso varies greatly, Neoteredo reynei having an unusually long heart in contrast to the remarkably short heart of Nausitora hedteyi. There is also considerable variation in the length of the ventricle in relation to that of the auricles. For example in Dicyathifer manni the ventricle is short, broad and inflated, but in Bactronophorus thoracites it is long and thin, the auricles in both are almost identical. I n Teredora princesae the ventricle is drawn out into a long tubular portion attaining a length almost three times that of the auricles whereas in Nausitora hedleyi and N . dunlopei where the heart has moved posteriorly along with the gills the auricles and the ventricles are of almost equal length. Also the auricles may be heavily pigmented as in Nausitora dunlopei, lightly pigmented as in N . hedleyi, or apparently not pigmented at all as in Teredofurcifera. Even though the general layout of the heart and the main blood vessels is generally similar, differences in detail are discernible. Thus Turner (1966) has noted in Teredppoculifer and Nototeredo norvagica that the tubular aorta extend anteriorly from the pericardium and branch just posterior to the posterior adductor muscle. In Spathoteredo and Nausitora the aorta immediately expands into a broad, thin-walled vessel which spreads over the dorsal surface of the visceral mass. Kuphus is unique in having a bulbous area anterior to the ventricle-the ventricular bulb separated by a large valve for the ventricle, the aorta opening from its dorsal surface and the intestine passing through it. Roch (1932) observed the pulsations of the heart in Teredo navalis. In the quiet animal the author counted one contraction every 2 sec at 17OC, when the animal was disturbed heart action stopped for 60-90 sec. I n Bankia indica (Nair, 1964) the heart pulsates at the rate of about 68 timeslmin when kept at room temperature (28-30°C). Manwell (1963) has shown the presence of myoglobin with concentrations of up to 2% in the adductor muscle of both Bankia and Teredo. Its presence is indicated by the pinkish hue especially of the posterior adductor muscle of live specimens. The presence of myo-

386

N.

BALAKRISHNAN NllIR AND M. SARASWATHY

globin is of advantage in view of the importance of these muscles in boring. Ansell and Nair (1968) demonstrated the occurrence of haemocoelic erythrocytes in the blood of Xylophuga dorsalis, the first record of these in a member of the Adesmacea. The isolated instances of the incidence of haemoglobin in solution in the haemolymph, in the ctenidium, and in the haemocoelic erythrocytes elsewhere in the Bivalvia have been reviewed by Read (1966). 11. The excretory system

Excretion is effected in shipworms as in other molluscs by two sets

of organs, the kidneys and the pericardial glands. Sigerfoos (1908) gave the first detailed description of the kidney in Bankia gouldi without mentioning the pericardial glands. Nair (1964) has described both kidney and pericardial glands in Bankia indica and Lane (1959) gave a brief account of the disposition of the renal organs in Teredo sp. Detailed descriptions of the kidney and the pericardial glands in Nausitora hedleyi, Teredo furcifera and Teredora princesae have been given by Saraswathy and Nair (1971). The kidney lies between the posterior adductor muscle and the visceralganglion above the pericardium. Behind the posterior adductor muscle the tubules (Fig. 24) form a compact mass below the anal canal.

FIa. 24. Nausitora hedleyi. Section passing through the tubules of the kidney showing the nature of the cells. ( x 147.)

THE BIOLOGY O F WOOD-BORING TEREDINID MOLLUSCS

387

Posteriorly four ducts are discernible, two afferent and two efferent renals. The kidney opens into the epibranchial chamber through the renal pores beneath the visceral ganglion. Communication with the pericardium is maintained through the afferent renal or reno-pericardial ducts by way of the reno-pericardial openings. White (1942) who described the pericardial glands in the lamellibranchs in detail, distinguished between an “ auricular ” position when the modified region of the pericardial wall is in close relation with the outer wall of the auricle and a ‘‘ pericardial ” position when the special-

Flu. 26. Nausitora hedleyi. Section through a part of the wall of the auricle to show the nature and extent of the pericardial glands. ( x 298.)

ized region lies inside the mantle at the side of the pericardium. According to her, both types sometimes occur in the same species. The auricular position is considered primitive and this condition persists in Bankia indica (Nair, 1964); Nausitora hedleyi, Teredo furcifera and Teredora princesae (Saraswathy and Nair, 1971). The auricles of N . hedleyi are highly pigmented owing to the investment of the thick layer of specialized tissue. In sections this appears to be made up of numerous closely packed rounded cells with a dense deposition of granules. Amidst the granules, muscle fibres are present and the granules appear to be arranged in rows. Cells charged with excretory matter drop into the pericardium and probably pass out through the kidneys.

388

N. BALAKRISHNAN NAIR

AND M. SAFCASWATHY

12. The nervous system

The disposition of the various nerve centres and nerves in the larva, the changes during growth and the nature of the system in adult Bankia gouldi have been described by Sigerfoos (1908), who found that Teredo navalis and T . dilatata conform to the same pattern. This is also true of Bankia indica (Nair, 1955). The cerebral ganglia are distinct, rounded bodies disposed dorso-lateral to the mouth behind the anterior adductor muscle and connected by a short commissure. The pedal ganglion is a single, compact body embedded within the tissues of the foot at its

FIG.26. Nausitora hedleyi. Section passing through the visceral ganglion. Note also the specialized portion of the proximal part of the reno-pericardial duct. ( x 148.)

mid-dorsal region just below the proximal part of the oesophagus. The cerebral ganglion of each side is connected to the pedal ganglion by a cerebro-pedal connective passing downwards on either side of the oesophagus. The visceral ganglion (Fig. 26) is the largest of the three ganglia and is flanked on either side by the dilated terminal portion of the reno-pericardial duct. The small " anterior ganglion ')described by Sigerfoos (1908) in Bankia gouldi is not represented in Nausitora hedleyi. Neuro-secretory cells occur in the Teredinidae and their cytology has been reported by Gabe and Rancurel (1958). I n the pholad Nartesia striata, Nagabhushanam (1965) noticed two types of neuro-

THE BIOLOQY OF WOOD-BORINQ TEREDINID MOLLUSCS

380

secretory cells, differing in size and staining properties, in both cerebral and visceral ganglia but only one type has been noticed in the pedal ganglia. The secretion is formed in four successive stages and the material is transported by way of the axons. 13. The reproductive system The gonads are symmetrical consisting of branching tubules which when mature form creamy white masses opening separately into the supra-branchial cavity by the gonopores through two short, wide ducts. The position of the gonad varies in different species and, as Turner (1966) states, " the position of the gonads appears to be primarily a matter of available space." The main body of the gonads may be posterior to the caecum as in Teredothyra matocotana, Nausitora fusticula and other species with a comparatively small caecum, or the gonad may extend along the dorsal side of the caecum as in Nausitora dunlopei. The gonopore is invariably situated at the posterior end of the pericardial cavity except in Kuphus. I n sexually mature Nausitora hedleyi the gonads occupy almost the entire available space within the mantle cavity and sometimes the tubules of the gonad are so crowded as to press closely against the neighbouring organs. I n ripe specimens collected during the breeding season, the part of the body behind the caecum may appear swollen on account of the great development of the gonad. The gonad is massive in a mature animal where the weight of this organ alone may form nearly half that of the entire animal. The gonad in Teredora princesae is also very conspicuous extending beyond the caecum. I n mature specimens the space behind the caecum between the gills is virtually packed with follicles of the gonad. I n the disposition of the gonad in relation to the visceral ganglion, T . princesae differs from N . hedleyi where the entire gonad even in very long specimens lies anterior to the visceral ganglion, with only the gonoducts passing beneath the ganglion to open behind it into the epibranchial cavity. On the basis of available information, tentative conclusions can be reached about the relation of the reproductive system to other structures in the mantle cavity. While the position of the gonopore is apparently constant, at the original site of the gonadal primordium adjacent to the visceral ganglion, the rest of the gonad extends according t o the available space. I n T . princesae the major part is distributed behind the visceral ganglion probably as a result of the curious horse-shoe shaped bending of the appendix and the consequent crowding of the organs in that region. In Teredo navalis the follicles of the gonad are distributed in the region in front of the visceral ganglion above the caecum. I n Bankia indica, while maintain-

390

N. BALAKRISHNAN NAIR AND M. SARASWATHY

ing the position of the gonopore near the visceral ganglion, the gonad extends not only anteriorly but some distance posteriorly as well. This can be explained on the basis of the position of the visceral ganglion, in this species placed approximately a third of the distance from the distal tip of the caecum. I n N . hedleyi the distribution of the gonadial follicles departs from the typical condition stretching for a considerable distance between the caecum and the gonopore. I n T . princesue this is short as in other shipworms and opens into the supra-branchial chamber and the follicles of the gonad spread above the appendix and beneath the ctenidia for some distance anteriorly as well. According to Sigerfoos (1908), the real " gonoduct " is remarkably short, formed as an ectodermal invagination soon after settlement the duct not breaking through till sexual maturity. I n Teredo furcifera the gonadial follicles even extend into the connective tissue of the mantle in certain regions. The major part of the gonad spreads over the caecum, the maturing follicles filling up the available space below the pericardium and posteriorly dilating so as to push aside the pericardium with its contained auricles. The gonoducts lie on the ventral side of the visceral ganglion.

IV. THE SEXUALPHASES As in many other Bivalvia (Fretter and Graham, 1964) sexual conditions vary widely in the Teredinidae. I n Teredo norvegica Yonge (1926b) noticed that the males were generally the smaller while the presence of two specimens containing both ova and spermatozoa indicated that this species is protandrous. Sigerfoos (1908) had already noted hermaphrodites among young specimens of Bankia gouldi and suspected the occurrence of protandry. Coe (1933-41) elucidated the sequence of sexual phases based on histological studies in Teredo, Bankia and Lyrodus. I n the first paper (1933) he revealed that T . navalis is a protandric hermaphrodite. The primary gonad contained both oogonia and spermatogenic cells, all individuals passing through an initial functional male phase and most of them later transforming into functional females with a small number persisting as true males. After assumption of the defhitive female phase, no evidence of a second sex reversal was noticed. Subsequently Coe (1934) showed the existence of a great disparity in sex ratios at different seasons of the year. (A change from the female phase to a second male phase was also reported by Coe (1934), according to whom animals which complete both sexual phases before the winter may repeat the succession of sexual phases in the next year.) Grave and Smith (1936) showed that in Teredo functional males constitute 30-50% of the adult population with a pre-

THE BIOLOGY O F WOOD-BORMQ TEREDINID MOLLUSCS

391

ponderance of functional males in young populations. Later a greater part of the individuals were found to produce eggs, these females having the ability to revert to the male phase. They also found that the transformation from female to male phase may occur abruptly during the breeding season as well as during the recuperation period and that gametes of both types capable of self fertilization may be produced in the same follicle. Coe (1936) showed the existence of a sequence of functional male and female phases in Teredo navalis-an initial functional male phase followed by a female phase, this often followed by a second male phase and sometimes by a second female phase. Some individuals remained in their first male phase for a long time or even indefinitely and these he named as true males. Coe (1941) later demonstrated protandry with a strong tendency towards rhythmical change of functional male and female phases in the larviparous Teredo diegensis and in the oviparous Bankia setacea. He came to the conclusions that (1) in Teredo diegensis functional hermaphroditism is common without any sharp demarcation of the sexual phases ; ( 2 ) in T . navalis functional hermaphroditism is not unusual, although the gonads are histologically ambisexual during the change of sexual phases ; (3) in Bankia setacea functional hermaphroditism occurs occasionally in the primary male phase but subsequent sexual phases are well defined and there is often a resting stage between them. Grave (1942) subsequently confirmed Coe’s data on the recurrent functional sex inversion in Teredo navalis but objected to his interpretation that Teredo is essentially or principally a protandric hermaphrodite. More recently Ganapati and Nagabhushanam (1954,1959),and Nair (1956) have shown similar sex changes in Teredo navalis, Bankia campanellata and B . indica from tropical habitats. Recent studies on a brackish water species Nausitora hedleyi (Figs. 27, 28) exhibiting a restricted breeding habit have shown evidence of an interesting sequence of sexual phases. These are of special interest since this species is one of the very few tropical molluscs with a restricted breeding habit owing t o the influence of salinity. Details regarding the sexual condition in specimens examined are presented in Table IV. There is a preponderance of ambisexual males among smaller individuals (1-50 mm) and as growth continues there is a tendency towards increase in the percentage of females with hermaphrodites appearing in the intermediate size group (50-200 mm). This suggests protandry and a probable change of sex from the initial bisexual male phase to the female phase. Of the 26 hermaphrodites examined only a few had gametes of both sexual types in the same follicle. Twenty-five were changing from the male to the female phase and one in the 250 to

392

N . BALAKRISHNAN NAIR AND M. SARASWATHY

FIO.27. Nausitora hedleyi. Section through a part of the gonad of an active male with running testes. ( x 300.)

FIG.28. Nausitora hedleyi. Section through a hermaphrodite gonad. ( x 300.)

300 mm size group was apparently changing from female to male, with the germinal epithelium proliferating spermatogonia and the lumen containing spermatozoa, a few ovocytes and ova. This specimen gave

TABLEIV. Nausitora hedleyi CONDITIONOF

Length group

True males

Ambisexual males

THE

Hermaphrodites

SEX OF SPECIMENS

Females

Immature

Total no. nf "J

in mm

1-50 . 50-100 . 100-150 . 150-200 200-250 . 250-300 . Above 300

.

No.

%

No.

yo

No.

%

No.

. . .

4 5 1

.

128 53 23 3 7 2 2

55.9 48-2 31.4 14.3 43.8 20.0 18-2

6 14 5 1 -

-

-

1.7 4.5 1.4 -

45 33 27 13 9 7 9

-

5.5 19.2 23-8 10 -

O/

/o

No.

19.7 30 37 61.9 56.2 70 81.8

52 13 8 -

-

o,

specimens

/O

22.7 11.8 11

-

-

229 110 73 21 16 10 11

394

N. BALAKRISHNAN NAIR AND M. SARASWATHY

evidence of a probable change from female to male during the breeding season as reported in Teredo navalis (Grave and Smith, 1936 ; Coe, 1936). Thus it appears that the proportion of individuals in the two functional sexual phases changes with the advance of the breeding season. There is a preponderance of ambisexual males at the beginning of the breeding season, with an increase in the number of females in the large size groups collected during the final phases of the breeding season, probably as a result of a change in sexual phases from male to female. There is a possibility of self fertilization during the intervening hermaphrodite period. A second sex reversal after the assumption of the definitive female phase (Fig. 29) may also occur. The conclusions reported above are drawn from the data collected during the breeding season of the species that extends from June to December ; the animals settled on test panels during July-August. From October onwards a small percentage of the females examined histologically showed indications of inactive gonads. There was noticeable reduction in the gametogenetic activity, at lowest level in late January and in February. During the non-breeding months, from January to May, specimens examined histologically revealed the presence ot the following categories of gonads. Indeterminate gonads where the follicles are not clear and sex not clearly determinable. The epithelium of the gonad apparently showed no sign of activity. Common during March-April. Among specimens distinguishable as females at least three types of histological conditions could be recognized. (1) Ova loose in the follicle with a few oocytes in the cortical region both undergoing a process of disintegration, and the epithelium apparently inactive : common during February. (2) Ova free in the lumen of the lobule with the walls containing proliferating spermatogonia. The cortical region is apparently active indicating a probable transition from a female to a male condition : in March. (3) Follicles shrunk but the cortical layer containing oocytes showing progress of oogenesis : in May, June and July. Two types of maIes could be distinguished during the non-breeding period: (1) with the cortical layer containing spermatogonia and spermatids and the germinal epithelium showing some activity, without sperms in any of the follicles, common in February; (2) with active spermatozoa free in the lumen of the lobule and the cortical layer with primary and secondary spermatids, with few differentiated oocytes representing an ambisexual gonad, common during May and June. Thus in Nausitora hedleyi in the estuarine locality of Cochin backwaters during the period January to May the gonads usually are in a state of apparent quiescence, The unspawned gonadial elements of the

THE BIOLOGY O F WOOD-BORING TEREDINID MOLLUSCS

395

PIO.29. Nuwitoru hedlkyi. Section through a part of the gonad in the active female phase. ( x 300.)

FIG.30. Nausitora hedleyi. Section of a hermaphrodite gonad giving evidenes of the concurrent production of gametes of both sexe8 in the same follicle. ( x 300.)

396

N . BALAKRISHNAN NAIR AND M. SARASWATHY

previous breeding season left in the follicles are probably resorbed and the epithelium undergoes a period of rest. By May or June gametogenic activity is particularly evident in the male phase and it is probable that these may provide the male gametes for the specimens bearing the type " 3 " gonad of the female recorded above. Thus in the Teredinidae three types of hermaphroditism may be distinguished, simultaneous hermaphroditism, consecutive hermaphroditism and rhythmical consecutive hermaphroditism (Fretter and Graham, 1964).

V. FECUNDITY Shipworms are prolific especially those that have external fertilization. These produce comparatively smaller eggs (around 45 p diameter). Teredo dilatata (= Psiloteredo megotara) produces over 100 million eggs in one spawning (Sigerfoos, 1908). The number of eggs and larvae produced by one Teredo navalis has been reported to exceed 2 million (Kofoid, 1921a). Imai, Hatanaka and Sat0 (1950) collected early veliger larvae of Teredo navalis from the gill chamber at the rate of 20 000 to 50 000 per individual. The values for Teredo furcifera from Bombay have been 7 000 for the first brood, the breeding potential increasing with age, one brood of an adult may contain more than 30 000 veligers (Karande et al., 1968).

VI. AGE OR SIZEAT SEXUALMATURITY Shipworms are known to attain sexual maturity quickly after settlement and metamorphosis. Bankia campanellata does so at a length of about 12 mm at Visakhapatnam (Nagabhushanam, 1959), Teredo (Lyrodus) mediolobata in Hawaii when only 10 mm long (Edmondson, 1942), and Teredo navalis at Sebastopol, Black Sea when 15-20 mm long (Bulatov, 1941). Teredo morsei (= T . navalis according to Moll) removed from ropes in New Haven, Connecticut was sexually mature when 10-12 mm long but those recovered from wood not until 40-50 mm (Coe, 1933a). T . navalis at Woods Hole is mature in 6 weeks (Grave, 1937). For T . parksi the age at sexual maturity is about 2 months in Samoa (Miller, 1924a) and 24 days at Pago Pago Harbour (Potts, 1923), for Lyrodw pedicellatus this period is nearly 8 weeks (Becker, 1959) while for the tropical Teredo furcifera it is only about 20 days (Karande et al., 1968; Karande and Pendsey, 1969). VII. BREEDINGSEASON Determination of the breeding period of the different species occurring in a locality is of particular significance. Of the several methods

THE BIOLOGY O F WOOD-BORING TEREDINID MOLLUSCS

397

employed for determining the breeding season of invertebrates, those widely used for shipworms have been (1) to observe the incidence of larvae based on regular collection of a given species from a known volume of water and the assessment of the density of larval populations during the different months in the plankton (Lebour, 1938 ; Nair, 1957 ; Quayle, 1953), and (2) t o determine the time of settlement based on a study of the relative abundance of post settlement stages in methodically operated test panels (Fraser, 1925; Johnson and Miller, 1935; Neave, 1943; Black and Elsey, 1947, 1947a, 1948; Ralph and Hurley, 1952 ; Nair, 1957, 1965, 1966 ; Saraswathy and Nair, 1969). This second method is of great practical significance since this alone provides a reliable measure of breeding success, there being the possibility of spawning without settlement. These methods are fairly reliable and useful in the case of marine forms and those that live in enclosed waters of a harbour. Nevertheless, they are not very reliable in special situations such as a harbour with typical estuarine conditions having oscillatory water movements with the influence of the tide a t one end and the inflow of fresh water a t the other complicating the water movements. To determine the exact breeding season of such estuarine forms (e.g. Nausitora hedleyi) Saraswathy (1967) employed a quantitative assessment of the condition of the gonad using the technique of gonad index developed by Giese and his collaborators (Bennet and Giese, 1955; Giese et a l . , 1959; Tucker and Giese, 1962; Giese et al., 1964). I n this method possibilities of errors due t o recruitment of larvae from marine sources are also excluded. A systematic examination of the gonad condition gives a fairly accurate picture of the breeding season. This method is based on the assumption that in individuals large enough t o be mature, a spent or immature gonad is small, whereas a ripe gonad is large. A gonad which decreases in size suddenly is assumed t o have lost its gametes-" spawned " (Giese, 1959). The gonad index provides accurate information on the breeding condition of individual animals and represents a measure of the reproductive condition of the p o p lation. I n the calculation of the index the gonad weight is expressed in terms of the percentage of the body weight. By the application of this method, not only can the individual reproductive condition be quantitatively assessed, but a graphic representation of the reproductive cycle of the species in question is possible. The data thus obtained may be supplemented with those drawn from the two other methods. The average values for the different months in the case of N . hedleyi (Table V) show that the gonad index is low during the period January t o June. For the rest of the period the values were above 15. The lowest value recorded was for June (4.99). The sudden decrease was probably owing

TABLEV. Nausitora Hedleyi, AVERAGEGONADTNDICES (G.I.) OF THE MALES, FEMALES AND SPECIMENS WITH INDETEKMINATE GONADS td

Month

No. examined

Average G.I. for the month

Male

Female

Indeterminate

No.

G.I.

No.

G.I.

No.

G.I. 0.52 g0na.d very small 11.49 10.68 11.87 4.65

--

November December January February March . April . May June July . August September October

.

. . .

.

.

. .

14 13 12 14

15.81 15.42 6.11 7.29

4 4 4 7

18.35 10.93 7-18 8.04

11 9 6 6

14.79 17.42 7.25 7.63

2 1

14 12 7 12 12 12 15 16

12.8 15.56 13.46 4.99 16.36 23.62 32.28 32.45

4 3 2 9 8 7 8

17.31 13.48 5-75 13.99 21.39 30.48 28.54

2 2 2 3 4 7 6

20.65 15.02 5.63 23.45 28.09 33.12 35.12

12 8 2 8 -

-

-

1 2

39.09 39.82

k

THE BIOLOGY O F WOOD-BORING TEREDINID MOLLUSCS

399

to an initial spawning which took place during that month. From this low index in June the values crept up steadily to a peak in October (32.45). Thereafter, the values showed a downward trend with a steep fall in November (15.81). In December also the value remained about that level followed by another major fall (6.11) in January. From January values showed a slight rise through February and March and reached a secondary peak in April. This was followed by a fall in values to the lowest recorded for the year in June. The data clearly show that N . hedleyi is not a continuous breeder in this locality. The high values noted for females during the months following June till October suggest very high activity of the ovary during this period. High gonad activity in N . hedZeyi is thus restricted, in this habitat, to a period of nearly 6 months from July to December. The peak period of settlement will, however, be slightly different from the period of maximum activity of the gonad since there is a time lag between spawning and the time of settlement. It is interesting to note that there is reasonable correlation between the data on the gonad index and the data collected from a system of test panels used to find out the time of settlement of the larvae. VIII. FERTILIZATION Three modes of fertilization have been recorded in the Teredinidae, (1) Egg and sperm separately extruded into the ambient water, fertilization taking place externally, (2) sperm discharged into the water by vile individual may be taken in through the inhalant siphon of another, fertilization taking place in the epibranchial cavity, and (3) the exhalant siphon of one (Fig. 31) may transfer the sperm directly into the inhalant siphon of another with the same consequence (Clapp, 1951 ; Turner, 1966). External fertilization of the type (1) occurs in Bankia setacea (Coe, 1941 ; Quayle, 1953) ; B. indica (Nair, 1956a) ; B. mmpanel-

FIG.31. Bankia gouldi, in the act of fertilizing its neighbour. Note the exhalant siphon of one inserted into the inhalant siphon of its neighbour. (AfterW. F. Clapp, 1961.)

B

R

C A O1

4

1

d2 B

%

C

MG

10

9

F

OD

AA

05mm

17

R

F

ss I'

FIG.32. Stages in the development of Bankia indica ( = B . carinata). (1) Surface view of the ripe ovum; (2) two-cell stage; (3) four-cell stage; (4) eight-cell stage; (5) twelve-cell stage ; (6) early stage in gastrulation; (7) eleven-hour-old larva after hatching ; (8) the trochophore larva ; (9) the early veliger ; (10) veliger larva on the eleventh day ; ( 1 1) late veliger on the fifteenth day ; (12) veliger larva on the fifteenth day with the valves and the mantle removed to show the internal organization; (13-14) right and left shell valves of the attached larva with one row of denticles ; (15) settled larva removed from the wood (not drawn to scale) ; (16) shell of the 2 mm-long shipworm ; (17) young shipworm 2 mm long ; (18) 2 mm long shipworm with the mantle and shell removed from the left side. AA, anterior adductor; BY, byssus thread; CEG, caecum of the stomach; DD, digestive diverticula; ES, exhalant siphon ; EN, endoderm ; F, foot ; G , gill ; I, intestine ; IS, inhalant siphon ; M, mouth ;MC, mantle cavity ;MES, mesodermal cells ; MG, midgut ; PA, posterior adductor; PB, preoral band of cilia; POB, post oral band of cilia; R, rectum; RM, retractor muscles ;SH, shell ;SHG, shell gland ; SO, sense organ ;SS, style sac ; ST, stomach ; STO, stomodaeal invagination ; V, velum ; VG, visceral ganglion. (After Nair, 1956.)

THE BIOLOGY O F WOOU-UOltlNO T E R l D l N l D MOLLUSCS

40 1

latu (Nagabhushanam, 1959) ; Nausitora dunlopei (Smith, 1963) ; N . hedleyi (Saraswathy, 1967) ; Nototeredo norvagica (Lebour, 1938, 1946) and Bankia gouldi (Sigerfoos, 1908). Fertilization of type (2) has been recorded for Lyrodus pedicellatus (Roch, 1940 ; Becker, 1959) ; L. diegensis (= L. pedicellatus) Kofoid et al., 1927) ; L. mediolobata (Edmondson, 1942) ; Teredo navalis (Grave, 1928) ; T . poculifer (Smith, 1963) and Lyrodus pedicellatus (=Teredo bartschi) (Isham and Tierney, 1953). According to Turner (1966) the following species may also be included since young larvae are present in the brood pouch of the parent, Teredo furcifera, T . parksi, T . somersi, T . clappi, Lyrodus afinis and L. massa. Turner feels that in Teredothyra matocotana and T . dorninicensis also fertilization occurs in the mantle cavity. Owing to the gregarious tendency in certain species (Nagabhushanam, 1959a) with settlement confined to susceptible areas of the wood, there are frequently localized concentrations of siphons on submerged timber. This probably increases the likelihood of sperm shed into the slowly moving water layer immediately adjacent to the surface of the wood, being taken into the mantle cavity of a female (Lane, 1955). He further suggests that insemination may be associated with interference with the normal respiratory stream or that the sperm themselves or fluids associated with them may cause retraction of the siphons and closure of the burrow. The fertilized ovum is retained in the maternal mantle cavity during early cleavage and later “ implants ” itself in the substance of the gill where early stages of development are completed. The third type of fertilization has been recorded by Clapp (1951) in Bankia gouldi. At Rovigno d’Istria, Roch ( 1940) tried breeding Lyrodus pedicellutus using running sea water and at Berlin Dahlem Becker (1959) reared this species in artificial sea water (temp. 20°C) for four generations and observed a noticeable lunar periodicity of spawning. Roch (1940)noted a pronounced rhythm in the extrusion of the larvae from the parent with a maximum at about 10 h before the astronomical full moon. During a lunar eclipse the spawning ceased and was resumed when the eclipse was over. Another maximum extrusion was observed at the time of the last quarter of the moon. Roch feels that this rhythm is neither dependent on the tides nor on the visibility of the moon. Becker and Schulze (1950) have described culture methods used in the rearing of Lyrodm. IX. EMBRYOLOGY AND LARVAL DEVELOPMENT A. The gametes Several species incubate eggs in the mantle cavity or the gill until they are developed as far as the free-swimming larval stage. Both this

402 N. BALAKRISHNAN NAIR AND M. SARASWATHY incubatory habit and hermaphroditism are, as suggested by Fretter and Graham (1964), related to the stress of reproduction in a habitat in some way unfavourable. The number of eggs produced is related to their size and yolkiness which in turn'depends on whether they are to be spawned in the ambient water for external fertilization or retained within the body of the female during early embryonic development. In the former case, they are usually numerous and small, in the latter fewer but larger. Thus the diameter of the mature egg of the oviparous species Bankia indica (=B. carinata) averages 45 p (Nair, 1956a), whereas that of the viviparous Teredo navalis has been given as ranging between 50 and 60 p (Loosanoff and Davis, 1963) which agrees with the measurements given by Jmgensen (1946) and Costello et al. (1957). Ripe eggs and sperms obtained from healthy individuals may be used for artificial fertilization t o obtain developmental stages. Early development of the egg of Bankia and other shipworms seems to be basically the same as that of other marine bivalves. Brief descriptions of this phase of development have been given by Quatrefages (1849), Hatschek (1880), Yonge (1924), Nair (1956a) and Costello et al. (1957).

B. Development I n Bankia indica early developmental stages were obtained through artificial fertilizations (Nair, 1956a) and the formation of the different stages (Fig. 32) is timed from the point of fertilization unless otherwise mentioned. The two celled stage is reached in about 50 min and within about 30 min after the completion of the first, the second cleavage, a meridional one, divides the micromere into two ; within 5 h, the embryo assumes a mosaic shape measuring 65 p. Gastrulation is by epiboly and takes place within 6 h after fertilization. When the gastrula is about 2 h old, the rudiments of the enteron and a few mesoderm cells are discernible in stained preparations. The stomodaeum is formed as a result of ectodermal invagination in the region where the blastopore has closed. Three hours later the proctodaeum is also distinguishable as another ectodermal invagination. The shell gland appears about this time on the dorsal side of the embryo and soon spreads out and the shell material deposited assumes the form of a cap covering the whole gland area. At this stage the embryo is elliptical in shape, 75 p in length and 52 p broad. The minute cilia covering its surface begin to beat and rotate the embryo. The free-swimming stage is reached about 11 h after fertilization. Sigerfoos (1908) found that Bankia god& hatches within 3 h. Quatrefages (1849) who studied the gametes and different phases of development of Teredofatalis ( = Notoferedonorvagica (Spengler 2)) collected at San Sebasti&nhas recorded the time required for the different phases of development such as from fecundation to the

403

THE BIOLOGY OF WOOD-BORING TEREDINID MOLLUSCS

extrusion of the polar body ( 2 li), from the extrusion of the polar body to the appearance of the cilia (9 h), and from the appearance of the cilia to the formation of the shell (81 h). Nevertheless, undue importance need not be given to the duration of difforent stages since development depends, among other factors, on the original condition of the egg, culturing methods, and temperature of the ambient medium (Loosanoff and Davis, 1963). In Bankia indica, 13 h after fertilization the larva becomes slightly broader at the anterior end assuming the shape of a top. I n addition to the feeble cilia developed all over the surface, conspicuous cilia develop along two distinct bands. A conspicuous pre-oral band of cilia, the prototroch is developed in front of the stomodaeal invagination composed of a double row of ciliated cells. A postoral band, parallel with the pre-oral belt composed of a single row of less conspicuous ciliated cells, is developed behind the stomodaeum. A third group of cilia is formednearthe proctodaeal invagination. This trochophore larva swims for nearly 8 h during the course of which a characteristic shell is secreted. In Bankia indica, when the trochophore is about 8 h old, i.e. within about 21 h after fertilization, it becomes the early veliger with a shell which can completely enclose the body. A pronounced development of the strong biserial band of preoral cilia takes place with the result that the anterior region of the larva enlarges. This area with its crown of motile cilia projects beyond the larval shell and is tho rudiment of the velum. The shell at this stage has a straight side, the " straight-hinge stage ", measuring 7 5 p in length and 60 p across. A median protuberance developed ventral to the stomodaeum represents the rudiment of the foot (Nair, 1956a). On the third day of development, i.e. about 7 2 h after fertilization, the straight-hinge larva has a much better developed velum with thickened edges bearing stronger and longer cilia. The shell gland spreads out with a consequent increase in the shell. Loosanoff and Davis (1963) describe the shells of straight hinge larvae of Teredo nuvalis as heavy and thick characterized by a dark band around the edge of the shell, and outside this a conspicuous light band. As the larvae approach settling size, the bands become less sharply delineated. The early larval shell is characteristically longer than wide, being 75 x 6 0 p to 90 x 7 0 p in Bankia indica (Nair, 1956); 95 x 8 0 p (Sullivan, 1948), 80 x 70 p (Loosanoff and Davis, 1963) or 85 x 7 2 p (Imai et al., 1950) in Teredo nawalis. Isham and Tierney (1953) record considerably higher values for T . pedicellata (245 & 2 0 p). The duration of the early veliger in the tropical oviparous Bankia indica is about 6 days during which it grows from 75 x 6 0 p t o 90 A.P.B.-9

14

404

N . BALAKRISHNAN NAIR AND M. SARASWATHY

x 70 p in size. Through allometric growth the valves assume a bulbous form around the eleventh day. By about 15 days the shell valves increase to 250 x 2 6 5 p the height becoming distinctly more than the length. The valves have bold and dark rims. It is interesting to note that the shape and nature of the valves of the late veliger of even such widely different genera as Teredo and Bankia seem to be remarkably similar (Sullivan, 1948 ; Quayle, 1953 ; Nair, 1956a ; Loosanoff, Davis and Chanley, 1966). The valves of these two genera are also similar in possessing three provincular teeth on the right valve and two on the left as also reported in Lyrodus pedicellatus by Rancurel (1951). The valves of the late veliger shell are equilateral, characteristically convex with high steeply slanting, narrow shoulders, prominent knob-like umbones, and short sharply curved bases (Nair, 1956a). Many authors have given essentially similar descriptions of the teredinid larvae (Sigerfoos, 1896, 1908 ; Borisjak, 1905 ; Nakazawa, 1915 ; Miyazaki, 1935 ; Lebour, 1938, 1946 ; Jarrgensen, 1946 ; Sullivan, 1948; Rees, 1950; Quayle, 1952; Isham and Tierney, 1953; Nab, 1956a). Nevertheless, the size at which free swimming planktonic larvae are ready for settlement varies. Thus, the late larvae of an oviparous species Teredo norvegica measure 380 p in length (Lebour, 1938), those of Bankia indica 273 x 265 p (height x length) on an average, those of the incubatory species, Teredo navalis 235 x 2 1 5 p (Imai et al., 1950) in Japanese waters and 250 x 220 p in Malpique Bay (Sullivan, 1948). The largest swimming larvae in the cultures of Loosanoff and Davis (1963) were approximately 231 x 200 p. The colour of the larvae darkens soon after they reach 1 O O p in length. The larvae of advanced stages of Teredo navalis do not develop an eye, the foot is extremely slender and worm-like and they attach themselves to the substratum by a byssus (Loosanoff and Davis, 1963). Imai et al. (1950) observed that neither foot, otocyst nor gill filaments appear before the larvae reach the size of 215 x 200 p but Loosanoff and Davis (1963) observed the appearance of these in larvae at least 15 p smaller. These larvae lead a pelagic life swimming actively and feeding on plankton. They are hardy, surviving in laboratory bowls in which the water was not changed for 9 days. The larvae of Bankia indica when about 17 days old are ready for settling on wood (Nair, 1956a). Preparatory to this they settle and then crawl on the surface of the wood pieces left in the container (Fig. 33). The period of crawling over the substratum varies greatly and may extend for up to an hour. During this period activity diminishes till the foot comes to rest in a depression on the surface of the wood. Subsequently the shell is lifted while byssal

TEE BIOLOGY OF WOOD-BORING TEREDINID MOLLUSCS

405

FIG. 33. Diagrammatic sketches showing the late veliger, pediveliger, arawling and boring stages.

attachment is made. The velum is then retracted. Larvae which were not 17 days old sometimes rested on the wood, crawling over the surface for some time and then extended the velum and swam off. At times the larvae remained motionless at the lower surface of the water adhering to the surface film. Disturbances of the medium such as stirring the surface resulted in the larvae withdrawing the velum for as long as 20-30 min and sinking passively to the bottom. After lying flat on one valve the foot was sometimes everted followed by crawling. Later, thrusting out the velum, larvae swam up towards the surface in a characteristic spiral manner. At this stage both the velum and the foot are functional so that larvae can alternately swim and crawl-a stage aptly termed " pediveliger " by Carriker (1956). If no wood was offered for settlement, the larvae swam about for a period of up to 9 days. I n such larvae the siphons grew and projected beyond the shell and 2-4 rows of denticulated ridges were developed on the anterior shell border suggesting a precocious preparation for settlement while still retaining larval characters. Thus, if a suitable substratum, namely of wood, is not available the free-swimminglarval life could be continued for several days. Loosanoff and Davis (1963) also noticed that the pediveliger stage may last under certain conditions, for several hours, or even days, as suggested by Thorson (1946), Nair (1956a), Wilson (1958) and others, postponing metamorphosis if conditions are unfavourable. This ability is probably of survival value permitting the larvae to cover a wide area in their search for the appropriate substratum. Nevertheless, Lane (1959) noticed in Teredo that larvae denied access to wood lost their ability to penetrate it within 4 days and invariably died with in 2 weeks. The infective period for this species was the first 96 h after release from the parent. During the period of 96 h when the larvae of T . pedicellata are infective they pass through quite marked morphological as well as

406

N. BALAKRISHNAN NAIR AND M. SARASWATHY

physiological changes (Lane, 1955). Observed swimming rates suggest that peak short-term velocity may approximate 7 mm per second. The shell valves do not contribute to swimming nor does the muscular foot.

C. Duration of the larval period The average duration of the free swimming stage of the veliger is apparently constant for a given species at a given locality. Naturally this period is shorter in the warmer waters of tropical and sub-tropical regions. The duration of the free swimming period in the non-incubatory species has been determined in a few cases. Sigerfoos (1908) suggested that veligers of Bankia gouldi swim about for a month or more at Beaufort and the same may be said of B. setacea (Tryon) occurring along the coast of British Columbia (Quayle, 1952). Nair (1956a) noted that in Bankia indica free swimming life is about 17 days in the tropical waters of Madras. For B. campanellata this period, according to Nagabhushanam (1959) is about 13 days. I n incubatory species, the duration of free swimming may range from a few hours to several days. According to Coe (1941) Lyrodus diegensis (=pedicellatus) has a brief free swimming period and some attached themselves to the substrate soon after release. Others in the same brood remained on the surface for 2 weeks or more before metamorphosis. Menzies (1951) concluded that larvae of T . diegensis must settle on wood within 24 h to develop into normal individuals. Failing this the shell becomes abnormal and they die within 2-6 weeks. The larvae of T. bartschi near Miami, Florida are free swimming for not more than 72 h (Lane, Tierney and Hennacy, 1954). Larvae of T . pedicellata remain free swimming for 3-4 days only at Miami (Isham and Tierney, 1953), while in Saint Mato and Dinard (English Channel) they do so only a few hours or days during which time there is no sign of growth (Rancurel, 1951). I n the waters of Barnegat Bay, New Jersey the free swimming stage of shipworm larvae is estimated t o last 3-4 weeks (Nelson, 1924). I n the tropical incubatory species T . furcifera larvae attack timber normally between 24-72 h (Karande et al., 1968). For T . navalis the free swimming stage is reported as between 24-34 days in Japanese waters (Imai et al., 1950) and about 24 weeks a t Woods Hole (Grave, 1928). Loosanoff and Davis (1963) cultured to metamorphosis, eggs and early stages of development taken from the gill chamber of T . navalis in 28 days a t a temperature of 20°C. However, the time required to reach metamorphosis varied, in some this occurred within 20 days after swarming when grown a t room temperatures. I n better growing conditions the free swimming period is shorter.

THE BIOLOGY OF WOOD-BORING TEREDINID MOLLUSUS

407

D. Food of the larvae Exact knowledge of the food of larvae is of great impoi tance if they are to be cultured. Most bivalve larvae need to feed during their free swimming stages and the provision of an adequate food is of utmost importance (Walne, 1964). Failure to raise larvae of bivalves by earlier investigators has been chiefly due to poor culture methods and want of suitable food. Diseases have also been responsible for such failures (Loosanoff and Davis, 1963). Yonge (1924) who reared the larvae of T. norvegica (Spengler) in Plymouth found that the larvae lived on their reserve food supply for as long a period as 14 days. Feeding on algae (diatoms) was also observed from the tenth day. Many bivalve larvae thrive on a diet of unicellular algae, sufficiently small to be swallowed and having a suitable nutritive value. Using a culture of the nonpigmented flagellate, Monas, Imai and Hatanaka (1949) and Imai, Hatanaka and Sat0 ( 1 950) successfully raised teredo larvae. However, Loosanoff and Davis, (1963) who give instructions about larvae rearing, and Walne (1956) consider that colourless flagellates are not good food for bivalve larvae. The activities of the larvae of T. bartschi Clapp previous to attachment to wood appear to rely mainly on glycogen stored in the oocytes and perhaps also obtained later from the maternal gill. During the first 24 h of free existence there is an increase in the rate of oxygen consumption (Lane and Greenfield, 1952)) probably owing to increased ciliary activity or to the operation of glycogenic enzyme systems which allow the completion of oxidative glycolysis. Then oxygen consumption decreases rapidly up to 72 h, and more slowly until the larvae die after about 300 h if they do not attain a suitable substrate (Lane et al., 1954). The large endowment of glycogen with which the zygote begins its existence is largely expended by the time the larva has penetrated wood (Lane and Greenfield, 1952). Apart from utilizing the stored glycogen, the larvae also feed on micro-organisms. Karande et al. (1968) on the other hand found that the larvae of T. furcifera need no food prior to settlement since larvae deprived of food by maintenance in sterilized filtered sea water have successfully bored into timber even after 4-5 days. The source of energy for the larvae has been attributed to the stored glycogen only (Lane, 1955).

E. Settlement Larvae are attracted to wood, at least in the sense that, should they chance to encounter it, they remain upon it and there metamorphose. This was established by Harrington (1922) who further suggested that malic acid was the active constituent responsible for this. Yonge (see

THE BIOLOGY OF WOOD-BORING TEREDINID MOLLUSCS

409

Barger, 1926) confirmed the former, but not the latter, conclusion. Further work on this is needed. Settlement of the larvae has been followed in certain species. I n T. pedicellata settlement takes place preferably after 24 and 48 h of free swimming existence (see Lane, 1955). On settlement the larva crawls actively with the aid of the foot and with its aid selects a satisfactory locus for penetration of the wood (Fig. 33). Isham and Tierney (1953) have shown that the wood must be properly conditioned for penetration and this involves among others saturation with water and the development of a suitable microflora and fauna (Becker and Kohlmeyer, 1958 ; Nair, 1965). In T. pedicellata Isham and Tierney (1953) report a profound change in behaviour 24 h after release from the parent (Fig. 33). The larva changes the mode of locomotion from swimming t o crawling over the available substrata using its highly mobile and sensory foot t o produce " a lurching locomotor pattern, searching, probing and prospecting the surface of the timber for a suitable locus for penetration ". During the process of penetration, according t o Lane (1955) " the shells are rocked rhythmically back and forth in a rough scraping movement, the foot meanwhile industrially sweeping the surface of the spot where penetration is t o occur. Before long, a small heap of debris is cleared from beneath the shells by the foot. This accumulates as a conical pile within which the larvae may still be observed t o move. The shell soon becomes calcified, teeth begin t o appear on the shell valves. Soon the animal becomes completely buried in the wood that is to constitute its shelter for the rest of its life." At the time of initial penetration, the larval shell valves are of conchyolin and without denticulations, the mobile foot is unarmed but the larva possesses considerable concentrations of cellulase even a t this stage. Taking all into consideration Lane (1959) concludes that initial penetration is accomplished by both mechanical and chemical means.

X. THE SEASON OF SETTLEMENT The time of settlement is of special interest apart from its biological importance because it is then that the infective free swimming larvae come into contact with fresh surfaces and experience the effect of preservatives used on them. Precise knowledge of the times of settlement of the different species in a locality is of importance in connection with such operations as replacements, dry docking and repainting of wooden boats, pile driving, etc. Biologically, the period and extent of settlement are significant since they are reflections of the breeding season and a reliable measure of their breeding success. This is due to the fact

410

N. BALAKRISHNAN NAIEt AND M, SmASWA'l'HY

that there is the possibility of spawning without settlement. In certaiB instances detailed studies on the season of settlement of timber boring organisms have shown effective ecological adjustments, the different species occurring in an area showing inter-relationships so that interspecific competition is reduced to a minimum through characteristio zonation in settlement (Nair, 1959). Alternation of breeding periods prevents simultaneous settlement, the different species occurring in the area settling over the limited amount of available timber at different times of the year leading to a succession in settlement (Nair, 1965). The breeding activities of closely allied species show differences and even those of the same may vary according to the hydrographic conditions prevailing in the area (Nagabhushanam, 1962 ; Nair, 1965). The density of distribution of shipworms has fluctuated over long periods and within the same period their attacks have differed considerably in various locations along the same stretch of coast line (Becker, 1958). This aspect of the activity of shipworms has been the subject of study in three localities along the coasts of India. At Cochin harbour, south-west coast, Nab (1965) observed that Teredo furcifera settles chiefly during the hot, highly saline pre-monsoon period, February to June, with sparse settlement during the early part of the monsoon and later part of the post-monsoon periods. The settlement of the estuarine species Nazcsitora hedleyi is confined to the low saline periods of the monsoon and post-monsoon periods (August-February) with apparently no settlement during the pre-monsoon. Thus, the settlement of these two species alternates in Cochin harbour. Nagabhushanam (1962) noted in Visakhapatnam (east coast of India) the occurrence of Teredofurcillatus ( T .furcifera)on test panels throughout the year with a maximum attack during the summer months between March and June with a peak in May during 1966. The difference noticeable in the nature of settlement along the south-west coast and the east coast of India may be explained on the basis of the prevailing hydrographic conditions. Beeson (1936) observed that the settlement of the free swimming larvae of Bartesia striata, a boring pholad, on test panels at the mouth of the Beypore river, south-west coast of India, is from November to June. The period of settlement of Bankia campanellata common at Visakhapatnam is from August till February and the species is absent from test panels during the period March to July, the maximum intensity of attack was noticed in November, December and January. Nagabhushanam (1962), pointed out a direct relationship between the relative abundance of shipworm settlement and temperature and salinity. The comparatively smaller attack rate by Teredo during the winter months (November-January) was attributed to a biological

THE BIOLOGY OF WOOD-BORING TEREDINID MOLLUSCS

411

competition with Bankia campanellata whose intensity was greatest during the winter months. Erlanson (1936) only found Teredo in the test blocks she used at Cochin harbour in spite of the fact that the period of her tests coincided with the breeding period of Nausitora hedleyi in the area. Since her tests were confined chiefly to the monsoon and post-monsoon periods (May-November), a period of very low salinity in the harbour when the breeding period of Martesia and Teredo was nearing completion, and since her test blocks were not attacked by Nausitora hedleyi she could not get a full picture of the magnitude of destruction by shipworms at Cochin harbour even though local people were fully aware of it. Erlanson (p. 731) concluded ‘‘ Contrary to local opinion the activity of molluscan borers in Cochin harbour and vicinity is less than elsewhere.” I

1

No 160-

140

-

120-

100 -

80 -

I

’

32 28

.24 -20 ’

16

60 -

12

40 -

8

20 -

4

FIG.35. Histograms representing the nature of settlement of Nuusitoru hedleyi on test panels. Short-term (shaded) and long-term (blank) during the different months at the pier of the Oceanographic Laboratory, Cochin. The graph presents the average gonad indices for the respective months.

412

N. BAIAKFtISHNAN NAIR AND M. SARASWATHY

TABLEVI. THE SEASONAL SETTL.EMENTOF SHIPWORMS ON SHORT-TERM PANELS (“A”SERIES)AT C o a m HARBOUR Nausitora hedleyi Panel No.

Period of immersion

Pre-monsoon 1st Feb.-1st Mar 1st March-1st April 1st April-1st May 1st May-1st June

Monsoon 1st June-1st July 1st July-1st Aug. 1st Aug.-lst Sept. 1st Sept.-1st Oct. Po8t-mo?tsoon 1st OCt.-lst NOV. 1st Nov.-1st Dec. 1st Dec.-lst Jan. 1st Jan.-1st Feb. Total for the year

,

InterSub- Bottom tidal tidal

A1 A 2 A 3 A 4

-

A1 A2 A3 A4

-

A1 A2 A3 A4

-

9

2

-

-

11

-

3

-

-

-

.3 6

7 21 9

15 43 11 3 81

31 9 1 90

9

Teredo fwcifera InterSub- B tidal tidal

11 35 30 81

159 217 145 113

-

-

7 13 179

o

607 305 340 268

2 14 26 12 49 667 1632

More recently Saraswathy and Nair (1969) investigated the settlement of N . hedleyi at Cochin harbour (Tables VI and VII). I n Table VI is presented the results obtained at Cochin harbour from an examination of the short-term blocks representing larval settlement during 30 days intervals of the pre-monsoon, the monsoon and the post-monsoon. To the question whether the settlement takes place in a restricted season or evenly throughout the year, this system provides a direct answer. Settlement of Nausitora hedleyi at Cochin harbour is seen as strictly seasonal. Since its inception in July, the settlement continued uninterruptedly till about February. The data also show that during this study, November represents a period of intense settlement with a period of fair settlement during August. Table V I I presents results from long-term blocks and indicates the progress of settlement .during the pre-monsoon, the monsoon and the post-monsoon periods. The general trend of settlement is the same in both series with little settlement during the pre-monsoon period. This set also shows how the monthly settlement may be modified when test

~

413

THE BIOLOGY OF WOOD-BORING TEREDINID MOLLUSCS

TABLEVII. T m SEASONAL SETTLE~N OBTSHIPWORMS ON LONG-TERM PANELS (“B” SERIES) AT COCHINHARBOUR Nausitora hedeyi

Period of immersion

Panel No.

Pre-monsoon 1st Feb.-1st March 1st Feb.-lst April 1st Feb.-1st May 1st Feb.-lst June

B1 B2 B3 B4

Molzsoon 1st June-1st 1st Jme-lst 1st June-1st 1st June-1st

B1 B2 B3 B4

July AUg. Sept. Oct.

Post-mowoon 1st Oct.-lst NOV. 1st 0ct.-1st Dec. 1st 0ct.-1st Jan. 1st Oct.-lst Feb. Total for the year

B1 B2 B3 B4

Teredo furcifera

InterInterSub- Bottom Sub- BoHom tidal tidal tidal tidal

-

3

-

-

-

-

17

14 29

9 43 67

2 127 39 28 239

16 193 223 213 763

-

-

-

11 23 13 21

2 7

49 62

-

9 138 207 220

-

706

1

-

11

9 98

169 76 111 94

607 221 434 487

6 43 3 26 14 93 No data

-

-

-

9 31 64 117 46 639 1991

panels are submerged for longer periods than 1 month and now the presence of organisms on the panels influences further settlement. The comparativelygreater number seen in the B2 than in A2 of the monsoon period not only illustrates this but also indicates the importance of the “ conditioning ” of the blocks through the interference of a suitable L r micro-flora ” which is known t o be an essential pre-requisite for the attack by marine borers (Becker and Kohlmeyer, 1958). The relatively greater number of specimens in panels of this set was due to longer exposure and so continuous settlement by waves of larvae during periods of immersion ranging from 1 month to 4 months. Based on a detailed study of the frequency of occurrence of veliger larvae in the plankton, the presence of post-settled stages on test panels and the condition of the gonads of the adults, Nair (1955, 1957) concluded that the period July-August is the best for larval development and settlement in Bankia indica (= B . carinata) at Madras (Fig. 36). The available data on the seasons of settlement are presented in Fig. 37, which has been compiled from the information furnished by

414

N. BAIAKRISENAX NATR AND N. SARASWAHY 11600

571

160C

144

128-

45-

120-

42-

112-

39-

104-

36-

96-

33-

c

g YI

L

X

88

- ;30TI)

8 0 - z 2772-’

24-

-

64-

21

56-

18-

48-

15-

40-

12-

32-

9-

24-

6-

16-

3-

8-

0-

0

-

Ripe female

*-------a Veliger larvae Settlement

FIQ.36.

Curves illustrating the occurrence of veliger lmvm in plankton, settlement of

spat on test planks (histograms)and the condition of the gonad of adult females of Badcia idea in respective months in Madras waters.

the various investigators using different methods without any uniformity in the exposure of panels, in their inspection, or in the identification of the species involved. It will be seen that in regions with marked seasonal changes in temperature settlement of many species is suppressed during the winter period. I n tropical conditions, seasonal changes in temperature are relatively small and settlement continues without interruption (Nair, 1957 ;Nagabhushanam, 1962). Even under such conditions the extent of settlement varies from month to month. I n special habitats such as estuaries, tbe influence of salinity may prevent the uninterrupted breeding and settlement of some species (Nair,

LOCALITY

India

,E

SPECIES

Coost

T. furcifera

I ----_-__I

India, E.Coast India, €.Coast India. SWCoost

Ecampanellato B. carinata T. furcifera

2+

4

N. hedleyi

5-

Burma, Rangoon

Bankia SP 6T. japonicaClessin 7 -

Japan

T. navolis B. setacea 8. setacea

Japan Pacific Coast of Canada Br. Columbia

Br. Columbia

3

-- -- - ------ -- - --- - -- __ - I

+---

Nair, N.B. sc0tt.c.w.

I

b------

-I

- I

-

I

I

9-

-----I?

I

c--------l

-------________________ *

Miyazaki, I.

Mawatari,S. White, F.D. Black, E.C.

S.FBay

B. setocea T navalis

12 -

Pacific Coast U.S.A. S.F:Bay

B. setocea

13-

Friday Harbour

8. setacea

14

Gulf Coast

Teredo navalis 7

15 -

Atluntic Coast U.SA. Beaufort N.C.

B.gouldi

16 -

I

I

Sigerfoos, C.P

Beaufort N.C.

T dilatata(=T.Knoxi) 17 -

I

I

Sigerfoos. C.P

Barnegat Bay, N.J.

T navalis

Pacific Cwst U.S.A.

I1

T. navalis

19

Teredo navalis

20 -

Wilmington,N.C. Wilmington,N.C.

Lymdus bipartita B.gouldi

21

22 -

Chesapeake Bay

8. gouldi

23 -

Pjlantic Coost,Camda,Prince Ed Is.

T navolis

24 -

NetherlonddHollond)

T novalis

25 -

I

T. megotara

26 -

France

T navalis

27 -

Denmark Hirtsholr

-

T megotara

28 -

Norway, S.W.Coast

Trnegotaro

Norway, Trandheim

T. megotara

29 30 -

Norway. S.WCwst

T narvegica T norvegica ? T norvegica

Putnam, J.W.

I

I

-----

t

-

I

- 1943

Scheltema and Truitt

4

c--.--l I

I

I

- 1918

Vr0lic.W. ef 01

- 1860

Levy-Salvador, I?Prudan,L. Kramp. P L .

-

1

I

I

I

I

I

31 -

Nair, N B. Dons, C.

Nair. N.B.

F

1

I

I

I

M

Orton, J H. Sbe Mundsson,B.

I

I

I I

A

I

I

M

J

I

J

I

I

A

S

1

O

I

N

- 1943 - 1944

Kindle,E.M. Redeke, H.C. I

- 1935 - 1880 - 1908

Richards. B.R. Richards, B.R.

I

J

- 1957

- 1965 - 1965 - 1932 - 1935 - 1950 - 1929 - 1934 - 1943 - 1927 - 1927

Richards,B R.

Grave. B.H.

I

I

I

3233 -

1962

- 1962

- 1908 - 1924 - 1937 - 1943

Nelsan,T.C.

c--lt-------l

-

Netherlands(Hal land)

England, Plymouth Iceland

Johnsan,M.W, Miller, R.C.

I

-

Massachusetts

Kofoid-Miller

{

18 -

Wi1rnington.N.C.

Neave, F Kofoid -Miller

I

I

-

-

.__-

8-

10

Nogabhushonam Noir, N.B. Nair. N.B.

-----

-__-_-_____________________ - 1

AUTHOR

Nogabhushonam

D

FIG.37. The season of settlement of various species of shipworms in different localities of the world.

- 1912-13 - 1930 - 1937 - 1962 - 1944 - 1962 - 1920 - 1903

416

N. BALAKRISHNAN NAIR AND M. SARASWATHY

1965). I n higher latitudes with rising temperature the breeding cycle is initiated and continues during the summer. Some attack almost continuously throughout the season, others vary in abundance in a way which suggests that successive generations are coming to maturity. The number of generations which would be produced in a single season varies with the time required for the species to grow to maturity and with the length of the period during which suitable conditions persist. I n temperate regions, a single generation may be produced in the course of a short summer. I n warmer regions development is more rapid and many generations may be produced each year. The seasonal breeding behaviour may be divided into a number of categories such as (1) settlement continuous throughout the year without definite seasonal fluctuations, (2) settlement continuous but with increased frequency during a definite portion of the year, (3) settlement limited to some definite portion of the year and (4) settlement occurring at two separated periods of the year. The first type occurs in areas such as the tropics where seasonal conditions vary only slightly and the normal breeding rhythms are apparently uninfluenced by them. This and the second category differ only in a quantitative way, the species concerned exhibiting definite variations in the frequency of settlement at different seasons. The second type may be expected wherever conditions during one portion of the year are less suitable for reproduction than at others. On the other hand in temperate regions where the annual change in temperature is relatively great the third type is usual, the duration of breeding depending on the time during which the temperature remains above the critical level for reproduction. Sometimes breeding may be interrupted in summer owing to temperatures rising too high, the species breeding in autumn or winter. This seems to be the case for Teredo norvegica in Western Norway (Nair, 1959, 1962). Again the season at which a given species breeds may differ in different parts of its range, e.g. in Teredo furcifera on the east and west coasts of India. Examination of Fig. 37 reveals this clearly for Teredo navalis, Bankia gouldi or B. setacea. The seasonal settling behaviour, therefore, depends on the time of the year at which conditions are favourable at a given place. It is not a fixed characteristic of a species throughout its range. Certain physiological races of Bankia setacea and Teredo navalis on the other hand are so limited in the range of temperature at which reproduction takes place that at some places they can breed only during a brief period during the yearly cycle when the conditions are favourable. This type of breeding occurs in places where seasonal changes in temperature are considerable.

THE BIOLOGY OF WOOD-BORING TEREDINID MOLLUSCS

417

It will be seen that temperature appears to be the principal condition determining the periods of breeding. Adult animals can fiequently survive under extremes of temperature which are unfavourable for reproduction. Consequently a species may maintain itself where conditions are suitable for reproduction during only a small part of the year In making generalizations one should not forget that variables other than temperature may be directly or indirectly influencing events. For example, especially along the south-west coast of India, rainfall reflects the passing seasons, causing great reduction of, as well as fluctuations in, salinity and so creating conditions unsuitable for breeding and settlement of certain species. Events leading t o settlement are dependent on the interplay of a large number of factors including the physiological characteristics of the species involved, their geographical distribution, local variations in the character of temperature changes and the seasonal influence of other and less obvious aspects of the environment. XI. THE PATTERN OF VERTICALSETTLEMENT I n the extensive literature on marine wood boring organisms only a few deal with the vertical distribution. This information is of considerable value since the degree of deterioration at different levels along a pile is based on the intensity of settlement and growth of boring animals at these levels. Further, a study of the varied biological relations which permit a heterogenous group of boring animals to share a common and limited habitat such as submerged timber will be of interest ecologically. Hobby (1918) noted on sample piles in the shallow waters of Manati Bay in eastern Cuba an increase in attack by shipworms from low water level to the mud line. Quicker deterioration at the mud-line has also been noticed by Johnson (1918) in the same area. McDougall (1943) noted at Beaufort, N. Carolina that infestation by Banlcia gouldi was heaviest near the mud line. Edmondson (1944) found out with the aid of test panels in Oahu, Hawaii that the shipworm attack was more severe on the deepest block at a depth of 74 ft than those at 50 or 25 ft. The species involved were Teredo milleri Dall, Bartsch and Rehder, Banlcia hwaiiensis Edmondson and Teredo trzclliformis Miller. At Miami it was observed that the frequency of attack by both Teredo and the crustacean Limnoria was on the average three times greater near the bottom than at the surface. Bankia and Nartesia were more evenly distributed. However, at two stations where salinity was highest, the pattern of attack was different being greatest at the surface (Budocks Technical Digest, 1950). At Loch Ryan in

A

0

FIG.38. A, Y a p of Vembanad Lake and Cochin backwaters, a typical tropical estuarine area along the south-west coast of India; B, map of Cochin harbour where studiee pn Nausitora hedleyi have been cmied out.

,

THE BIOLOGY O F WOOD-BORING TEREDINID MOLLUSCS

419

south-west Scotland, Owen (1953a) observed that the larvae of Teredo norvegica Spengler tend t o settle in increased numbers in dimly lit regions and that there is an obvious increase in the number of entry holes with increase in depth, maximum attack being noticed a t the mud-line about 30 ft below mean tide level. Generally in shallow waters the strike of teredines increases with depth (Kofoid et al., 1927 ; Johnson and Miller, 1935 ; Edmondson, 1942 ; Black and Elsey, 1948 ; Greenfield, 1952; Nair, 1966). Quayle (1953) who studied the distribution of larvae of Bankia setacea in British Columbia found that the number of larvae increases with depth. Information regarding this important aspect of activity of marine borers has been scanty from the Indian Ocean area. At Visakhapatnam, India, Ganapati and Nagabhushanam (1955) studied the vertical distribution of Martesia striata. They noticed a definite increase in the number of entry holes from the high tide level down t o about 3 ft below the low tide mark below which there was a sharp decline down t o the mud-line. The maximum intensity of attack was in the 3-ft zone above and below low water mark. It is well known that the relations of closely allied species are different and even those of the same may vary according t o the hydrographic conditions locally prevailing (Clapp, 1935; somme, 1940), each species of borer having its own characteristic preferences, life history and seasons of settlement. Earlier studies have been chiefly based on random observations on piles pulled out from harbours reporting the activity of either the molluscan or crustacean borers and no effort has been made t o study the combined activity of the different species of borers in a locality. Generally these animals work together in their destruction of wood in close association with a variety of fouling organisms. An attempt t o study the nature of destruction by all the boring animals was made by Nair (1966) a t Cochin harbour (Fig. 38), a typical tropical estuarine habitat on the south-west coast of India. The pattern of distribution was found t o be similar t o that observed a t Beaufort, a t Loch Ryan, Manati Bay or Oahu, the deepest blocks registering the most severe attack. I n the case of the estuarine species Nausitora hedleyi, significant differences have been noticed in the intensity of settlement at the different levels during the different periods of the year (Nair, 1966; Saraswathy and Nair, 1969). The data presented in Tables VI and VTI besides providing details regarding seasonal settlement, also give information on the vertical distribution a t intertidal and subtidal levels and on the bottom for all the three significant periods of the year. The pre-monsoon is a period when the salinity is fairly uniform and high with little difference between the surface and the bottom (Ramamir-

420

N. BALAKRISHNAN NAIR AND

M. SARASWATHY

tham and Jayaraman, 1963). The monsoon period (Fig. 39) is characterized by very low salinity values especially at the surface owing to the large inflow of fresh water and the influx of sea water constitutes only a distinct bottom layer. During the post-monsoon period the salinity shows an upward trend with fluctuations and the difference between the surface and the bottom values tends to diminish. With this picture of the prevailing salinities, a scrutiny of the tables (VI and 1963

I964

I965

300.

800. 900-

*C

- 33

.27

0N D J F M A M J J A S O N D J F M A M J J A i b N D

FIG. 39. Temperature, salinity and rainfall data for a typical tropical estuary, the habitat of Nausitora hedkyi. A, average salinity (surfme, Ernakulm channel); B, average maximum atmospheric temperature ;C, average minimum atmospheric temperature; D, average water temperature (surf-), Emctkulem channel.

THE BIOLOGY OF WOOD-BORING TEREDINID MOUUSCS

421

VII) will suggest probable causes for the differences in the pattern of vertical distribution. During the monsoon period distinctly greater numbers settled over the bottom panels. During the post-monsoon period the nature of settlement was different with the sub-tidal panels giving evidence of a greater strike than the bottom panels. This naturally suggests a shift in the nature of settlement owing to the overriding influence of some ecological factor, most probably salinity. The trend is almost the same in the long-term panels also and serves to ctonfirm the results obtained from the short-term panels. In Table VIII and in Fig. 40 are presented the results of a conTABLEVIII. N a u e i t o r a hedleyi, THE NATURE OF THE VERTICAL DISTRIBUTION DURINQ THE MONSOON AND THE POST-MONSOON PERIODS

immersion

Date of colleotion

20.6.1965 20.6.1966 20.6.1965 20.6.1966 20.6.1965 20.6.1965 15.10.1965 15.10.1965 16.10.1965 15.10.1966 16.10.1965 15.10.1965

5.10.1965 6.10.1965 5.10.1966 5.10.1965 5.10.1966 5.10.1965 3.1.1966 3.1.1966 3.1.1966 3.1.1966 3.1.1966 3.1.1966

Date of

Position of panel above mud line i n cm

Number of epecimens on Panel

270 230 180 130

14 15 37 19 38 72 210 536 472 494 417 219

80

30 270 230 180 130 80 30

h a t o r y test carried out with a view t o checking the details of the difference noticed in the short-term and long-term series. The pattern of settlement is different during the low salinity period of the monsoon (A) and during the post-monsoon period (B) when salinity shows an upward trend. While the pattern during the first test (June-October) is suggestive of an apparent increase in larval strike towards the bottom Qhisis not so for the second test (OctoberJanuary). Here maximum mttlement is towards the upper levels and minimum numbers occur in both the bottom and topmost panels. The apparent change in the pattern of settlement suggests that vertical distribution is not based on a set behavioural pattern but depends also on such factors as the distribution of salinity in the surrounding water. It was not evident from these tests whether the larvae were distributed equally throughout the

422

N. BALAKRZSHNAN NAIE AND M. SARASWATHY

20 -

70120

-

170-

220 270

-

I

- 14 - 15 A

- 37 - 19

- 30 - 72

- 210 ‘36

- 472

- 494 B -417 -219

FIG. 40. Vertical distribution of Nawitom hedleyi during the monsoon and postmonsoon periods. Numbers at the left of each profile indicate depth in am. (the bottom panel was a t e level 30 cm above the mud line). At right ia shown the average number of specimens at the depth indicated. A, results of test during the monsoon period, panels exposed on 20 June 1966 and collected on 6 October 1966; B, results of test during the post-monsoon period. Panels exposed on 16 October 1966 end collected on 3 January 1966.

water column and only those at certain levels were successful in settling and surviving, giving the impression of greater settlement at those levels. Nevertheless, in the Cochin backwaters July t o October is 8 period of low surface salinity. I n Fig. 41 two sets of data are presented on the differences in salinity at the two levels taken at hourly intervah over 24h during the post-monsoon period, one for 9.10.1965 and the other for 8.11.1965. Tests on the influence of salinity (wide infra)on development have shown that salinities below about S%, are higbly unfavourable. Since the prevailing surface salinity during the period of the first test was much less than could normally be tolerated, it is easy to understand the comparatively greater settlement towards the bottom where the salinity is higher. During the period of the second test the surface salinity was altogether different from that during the first test. During October and November, the average values were 10.77%,, and 16~92% respectively, ~ both suitable for the species. In this instance it

THE BIOLOGY OF WOOD-BORING TEREDINID MOLLUSOS

423

FIU. 41. Curves illustrating the hourly fluctuations in the salinity of the Ernakulrtm channel. (1) surface; (2) two-metre depth. A, data collected on 9 October 1965; B, data collected on 8 November 1966.

was probably the comparatively higher salinity at the bottom that inhibited greater settlement at that level so producing an opposite result to that noted in the fist test. Further, the disparity between settlement at the two levels, top and bottom, is not so conspicuous in the second test. This is probably the result of the comparatively small difference between salinity values at the top and bottom levels. Our data suggest that in the shallow waters of Cochin N . hedleyi shows significant differences in the intensity of settlement at different levels during the different periods of the year. This suggests that borer activity though generally considered most abundant near the bottom need not necessarily be so at all locations. In waters which are predominantly fresh with the exception of a more saline layer at the mudline resulting from tidal action, Teredo pedicellata were more apparent

424

N. BALAKRISHNAN NAIR AND M. SARASWATHY

near the bottom (Greenfield, 1952). I n a station where there was uniform salinity at all depths, the species occurred in great numbers at the surface. I n another locality at the mouth of the Miami river where there was uniform attack by borers throughout the vertical column, the salinity was found to be higher than up river with the surface layer showing evidence of dilution with fresh water (Greenfield, 1952). The vertical distribution of shipworms may also be influenced by other factors. Isham et al. (1951) noticed maximum attack at 166 ft candles decreasing at both higher and lower light intensities. Owen (1953a) observed greater attack by Teredo norvegica with increase in depth and in dimly lit regions of Loch Ryan. According t o Rancurel (1951) larvae of T . pedicellata are photopositive up to metamorphosis and Greenfield (1952) has suggested the effect of a negative geotactic response. More reliable information on vertical distribution can be obtained by selecting suitable test sites at several places in an estuary and by following the effects of salt water intrusion and other factors. Data obtained from piles and poles removed from a harbour area after being in water for several years may not give a reliable picture of the sequence of events that take place in regard to larval settlement. They reveal only the total attack by a variety of borers under the influence of the prevailing physical, chemical and biological factors during the period the pile was in water. Examination of the pattern of distribution based on panels exposed for long periods of time and involving more than one species of borer is also likely t o present only a general picture. Detailed observations with a methodically operated system of panels side by side with examination of hydrographical data alone can ensure reliable conclusions about the pattern of distribution. Differences in the magnitude of the strike is probable in the same locality even in successive years but the nature of relationship of the different species t o the combination of environmental factors may be almost the same. XII. TEREDINIDSIN DEEP WATER Shipworms are not confined to shallow coastal waters where, through the agency of man, they have access t o a greater amount of substrata than elsewhere in the sea. Shipworms do also occur in deep water. Bartsch (1927) has collected and described several species from dredged pieces of timber obtained by the Albatross Philippine Expedition in depths ranging from 51-548 m. Roch (1940) records Teredo utriculus ( =Nototeredo norvagica according t o Turner) recovered from the jute layer of a cable removed from a depth of 700 m. Turner (1966) reports the occurrence of Bankia carinata (Gray)at 7 488 m in the Banda Sea, Uperotus clavus (Gmelin) from pandanus fruit at the same station,

THE BIOLOGY O F WOOD-BORING TEREDINID MOLLUSCS

425

Lyrodus bipartita (Jeffreys) from the Gulf of Panama in 3 710 m and Teredothyra smithi (Bartsch) from 5 050 m in the Sulu Sea. These records are from the wood dredged by the Danish research vessel “ Galathea ”. The Atlantique Sud Expedition had also collected Bankia carinata from different depths, in 250 m near Port Gentil, Congo, in 200 m about 40 miles WSW of Mouta Secca Point, Congo, and in 145 m about 35 miles west of Ambrizette, Congo. Nototeredo norwqica had been dredged from 944m by HMS “Triton” off the north coast of Scotland. Bankia carinata, Teredothyra atwoodi and T . docotana have also been collected from test boards about 2 miles east of Fort Lauderdale, Florida in depths o f 100 m (Turner, 1966). Our information about teredinids from deep water is thus very limited and fragmentary. It will be seen that many of the species that occur in deep water also occur in shallow waters. These findings, however, suggest that teredinids are able to settle, grow and reproduce at considerable depths. XIII. GROWTHRATES Studies on growth rates are important because they are directly related to the damage done to timber. Each shipworm destroys a column of wood of the same dimension as its largest size. The use of X-ray photography (Ralph and Hurley, 1952) and the utilization of sterioradiography (Crisp et al., 1953) have facilitated the study of growth rates of their calcium-lined burrows without damaging the substrate or disturbing the animals. Comparisons of growth rates of different species o f shipworms recorded from different kinds of timber from different localities do not seem to have much meaning. The growth rates of different species occurring in widely separated places are likely to be different and even in the consideration of growth rates of the same species, unless the latitude, substrate involved etc. are the same the values are likely to vary. Growth rates need not be identical even when latitude, species and substrate are all the same during the different seasons since they are likely to be influenced by the prevailing hydrographic conditions. Further, Scheltema and Truitt (1954) observed that Bankia gouldi has different rates of growth at different localities of the same estuary during the same time depending on the number of individuals which have settled. Despite these factors, a brief review of the results of growth rate studies appears justified. In Bankia setacea an average rate of boring of about 4.7 cm/month was noted by Kofoid et al. (1927) ; at Friday Harbour, Johnson and Miller (1935) observed that the largest specimen of B. setacea measured

42 6

N . BALAKRISRNAN NAIR AND M. SARASWATHY

3 9 cm long from a block which had been immersed from September to January, while from British Columbia, Quayle (1959) reported a mean monthly increase of 12.2 cm in one specimen which attained a length of 61.0 cm in about 5 months. I n Woods Hole, Grave (1928) noted growth in length of Teredo navalis as follows : 0-35-0.5 mm in 18 days, 8-10 mm in 33 days, 100-120 mm in 72 days to reach a length of 250-400 mm in one year. Miller (1922) observed in T . navalis that the rate of growth as measured by the addition of ridges is extremely rapid during the first month (9.3) after which it stops suddenly remaining nearly constant during the next 2 months (3.8-3.6) followed by a further decrease during the fourth month (2.6). He suggested that the decrease is due either t o the lowering of temperature or t o the effects of crowding, limiting further growth. According t o Richards (1943) the growth rate in N. Carolina for T . navalis is 10-30mm and for Lyrodus bipartita 10-15 mm during the period May-January. Sigerfoos (1908) observed in Bankia gouldi from N. Carolina a growth of 3 mm in 12 days, 6 mm in 16 days, 11 mm in 20 days, 63 mm in 30 days and 100 mm in 36 days. This represents a higher growth rate than what Richards and Clapp (1944) reported for the same species from Florida waters and a little less than that reported by Richards (1943) from Wilmington, N. Carolina (35-125 mm). For Teredo megotara, & (1927) noted at Hirtshals a growth of 15 cm for 6 months and 26 cm for 1 year. However, Dons (1940) obtained a t Trondheim, Norway, different values namely 37 cm in 6 months and 52 cm in 1 year and Nair (1962) observed a maximum length of 28.6 cm for a period of about 5 months for this species at Espegrend in western Norway. For Bankia australis Ralph and Hurley (1952) recorded growth in length of about 45 cm in 1 year. They obtained an ordinary growth curve which showed a deceleration of growth rate in September and again in November, i.e. in winter and in spring. This feature has been noticed by Isham et al. (1951) in Teredo pedicellata at Florida. While in T . pedicellata this was attributed to the effect of overcrowding, in Bankia australis the deviation of the curve was interpreted as due t o individual variation. According to Lane (1959), the average life span of Teredo in Miami is about 10 weeks during which time it grows to a length of 100-125 mm and a diameter of 0.25 mm. Johnson et al. (1936) noted a diameter of & i n at the end of 3 months growth for 3 Australian species. As early as 1923, Bartsch proposed a new term " stenomorph " for shipworms that are dwarfed as a result of overcrowding and consequent lack of sufficient space for normal growth. Despite this stunted growth, he observed that these dwarfs attain sexual maturity. Clapp (1925) also recorded such stenomorphs and pointed out that while these may

THE BIOLOGY O F WOOD-BORING TEREDINID MOLLUSCS

427

live as long as normal ones, they are unable to increase the length or diameter of their tubes. Their only growth, he observed, was a regular addition of the denticulate ridges and an increase in the thickness of the shell and abnormalities in the nature and the relative proportions of the different parts of the shell. While normal specimens grew t o a length of 10 mm in less than 2 weeks time, stenomorplzs, even a t the age of 10 months remained unchanged a t this length. Edmondson (1942) noted " stenomorphic forms in Teredo milleri and T . gregoreyi from Hawaii. I n Bankia indica of Madras, the growth as reported by Nair (1960) is 9 mm in 17 days, 23 mm in 32 days, 142 mm in 68 days, 224 mm in 95 days, 257 mm in 125 days, 274 mm in 165 days, 290 mm in 191 days and 302 mm in 219 days, representing an average rate of boring of 4.3 cmlmonth. Data on growth in length of the animal, growth in the size of the shell, increase in the number of ridges on the shell valves and increase in the weight of the animal indicate that growth is very rapid during the first 90 days and thereafter slackens and the trend indicates that growth becomes negligible a t the end of about 220days. Retardation of growth has been attributed t o depletion of the woody material on the panel as a result of overcrowding. Growth rate studies on B. campanellata (Nagabhushanam, 1959) revealed a growth of nearly 51.5 mm/month. Maximum growth during the year was recorded in December when the burrow length increased by 60 mm. Teredo furcillatus in Visakhapatnam harbour was found t o reach a maximum of 90 mm, dry weight 110 mg and wet weight 319 mg at the end of 5 months. Maximum growth was recorded in May when the burrow length increased by about 29 mm. Maximum growth coincided with the highest temperature, i.e. 30-9"C (Nagabhushanam, 1961). We assessed the growth of the estuarine N . hedleyi in the indigenous timber Hangifera indica. The length of the burrow, wet and dry weights of the animal, weight of the shells and of the pallets, the number of denticulated ridges over the shell, length and height of the shell, proportion of the pallet blade and stalk and the number of cones that form the blade were all considered over a period of nearly 6 months. The salient features of the growth rates of this species assessed on the basis of the above characters were as follows : growth was rapid during the period between 45 and 135 days after settlement (13.9.65to 12.12.65) with the maximum growth between 105 and 120 days of age. Thereafter, growth slackened and the trend indicated that growth was negligible a t the end of 150 days. This might be owing t o retardation in growth as a result of the effects of overcrowding and the depletion of the substrate preventing further boring. It might also be the effect of an increasing and unfavourable salinity. While reasonably valid cor))

428

N. BALAKRISHNAN NAIR AND M. SARASWATHY

relations have been obtained with reference to burrow length and time, number of cones on pallets and time, wet weight and length, dry weight and length and between the number of pallet cones and the number of ridges on the shell, no such relation was evident between pallet length and burrow length as obtained by Hurley (1959) for Bankia australis wherein 1 mm of pallet length was found to represent 1 cm of total length (as indicated by burrow length). Failure to obtain valid correlation between these two characters was probably due t o the slackening of growth in length owing to overcrowding, while the pallets continued growth after that of the body had ceased. During the period of maximum growth, the salinity remained between 8 and 20%,. Below and above this range growth was negligible. XIV. DISPERSAL OF SHIPWORMS Notwithstanding the stationary, hidden life within the confines of their wooden burrows, shipworms are distributed far and wide through their free-swimming larval stages. While some species liberate eggs into the water, others brood the eggs, the veligers being releasedwhenready. During the free-swimming period which may last from a few hours to even a month depending on the species and the region, the larvae are drifted about and widely transported in the surface currents. Three types of larval life could be recognized among shipworms: (1) oviparous ; (2) short-term larviparous ; (3) long-term larviparous. The pattern of distribution of many species is based on the temperature and salinity requirements of the larvae during their planktotrophic life. The members of the genus Nausitora, generally denizens of brackish water habitats, are oviparous and fertilization is external (Watson et al., 1936; Smith, 1963; Saraswathy, 1967). Since the larvae are incapable of tolerating high salinities (Saraswathy, 1967), those larvae transported by the medium into areas of high salinities would perish. This accounts for their occurrence in isolated pockets of brackish water. In this case colonization of new areas could be effected only by the adults which are more tolerant of higher salinities than their planktonic larvae and are transported through the agency of driftwood etc., to a suitable brackish-water environment within the lifetime of the adult. The picture of the distribution of this genus seems to support this contention. Nausitora hedleyi and N . dunlopei have so far been reported only from isolated brackish-water areas along the tropical Indo-west Pacific, N . dryas and N . excolpa along the tropical eastern Pacific and N . fusticula along the tropical western Atlantic. Species of Bankia are also oviparous with protracted planktotrophic larval stages but their habitat is normally marine. I n this case the

THE BIOLOGY OF WOOD-BORING TEREDINID MOLLUSCS

429

limiting factor in distribution is apparently temperature. Therefore, species characteristic of higher latitudes are restricted in range, incapable of spreading into sub-tropical or tropical areas as may be seen in the case of Bankia setacea of eastern and northern Pacific, B. gouldi of northern and western Atlantic and B. martensi of southern South America and South Africa. Similarly the tropical species B. carinata, B. campanellata and B. bipennata, though established all round the world are restricted by the temperature factor and have not spread beyond the subtropical zone. While discussing the dispersal of marine species with long-term larviparous young such as the members of the genus Lyrodus and Teredo furcifera, T . clappi, T . somersi and T . bartschi, Turner (1966) enumerates the reasons for their world-wide distribution : (1)in common with other shipworms the adults can be transported great distances in ships or floating wood; (2) the young are protected within the parents during the early critical stages of development ; (3) the larvae are not spawned unless optimal conditions for their survival exist ; (4) being further developed, the young are less sensitive when extruded; ( 5 ) the larvae are ready t o settle shortly after they are extruded and so are not carried away from the floating log or ship from which they emerged ; and (6) most wooden ships and pieces of driftwood are covered with a good growth of hydroids, bryozoans, algae and other organisms which form a protective " forest cover within which the larvae can swim until time of settlement ". The wide distribution of Teredo navalis, which is a short-term larviparous species, is because it is both eurythermal and euryhaline while the restricted distribution of the larviparous species T . poculifer is due to its brackish-water habitat. Protection t o the larvae is afforded by retaining them until the late veliger stage within the mantle cavity and through an ephemeral free-swimming stage which lasts only for about 24 h. Experimental studies on the dispersal of shipworms have been few. By far the most common ways have been by driftwood or through the agency of the wooden hulls of ships, etc. Some believe that Teredo was brought to Holland, England, and other European countries by wooden vessels from the tropics, possibly from India (Brown, 1816). However, fossil records do not support this view (Deshayes, 1860; Jeffreys, 1861). There is no doubt that extended and intensive intercourse between nations in the long years of maritime activity contributed t o the spread of this menace in widely separated places. Historical records indicate that marine borer attack had increased in Pacific coast harbours with the increase in shipping, the chief agents in transport being the hulls

430

N. BALAKRISHNAN NAIR AND M. SARASWA!lV3Y

of wooden ships, wooden sea water tanks of ships and log-booms (see Kirkbride, 1922 ; Moll, 1936, 1936a). Rapid increase in maritime ship ping in the past two centuries helped this transport (Kofoid et al., 1927). The European species reached American shores during World War I (Brown, 1935). Ships transported at least one species to South Africa, China, Japan and Australia (Moll, 1936, 1948). It is also true that infested driftwood carried by the surface currents played a major role in their wide distribution (Moll, 1940, 1941). Floating nuts and seeds drifting passively in the surface currents distributed at least one nut-infesting species in the region between the east coast of Africa and the Philippines (Moll, 1936, 1948; Moll and Roch, 1937). From the Philippines and neighbouring areas many species have reached Hawaii in driftwood (Moll, 1941) and in light ocean-going craft of wooden construction (Edmondson, 1946a, 194613, 1962 ;Mawatari, 1950). The whole Indo-west Pacific area contains many common species (vide Table 111). There is also the possibility of the release of larvae from infested waterlogged wood lying on the sea bottom. This picture of wide distribution can be explained either on the basis of passive dispersal of free-swimming larvae and of adults through prevailing surface currents and drif'twood respectively or through the active transport of adults by ships. Thus a few tropical species such as Bankia carinata, B . campanellah and B. bipennata have succeeded in establishing themselves around the world in both tropical and subtropical waters. It has also been noted that the larvae can be effectively transported amidst the thick growth of fouling organisms that accumulate over the bottoms of the steel hulls of ships. A curious means of transport of larvae within the body of a fouling organism has also been recorded. Larvae taken in with the feeding current in one locality by a worm attached to a ship passed through the alimentary canal apparently undamaged and emerged alive along with the faecal pellets of the worm when the ship reached another locality (see Turner, 1966). These observations reveal that several species of shipworms have been dispersed, and others may be expected to be so, over wide areas of the oceans. Edmondson (1962) reports that certain shipworms can spend the life cycle from larva to adult in the open sea supported by some suitable flotsam without making contact with stationary structures in coastal waters. The larvae of these " seasoned ocean travellers " can endure long enough to contact drifting timber and continue a chain of seafaring generations.. As pointed out by Edmondson (1946) while specimens from drift logs and wooden hulls may serve as a legitimate record of the locality, they may not represent established fauna. Conditions must be sufficently suitable for spawning, for the survival of the larvae and success-

THE BIOLOUY O F WOOD-BORING TEREDINID MOLLUSCS

431

ful penetration of the wood before a species can become an established member of any local fauna (Turner, 1966).

XV. PHYSIOLOGICAL STUDIES That the shipworms have not been favourite objects of physiological work is evident from the fact that the recent review " Physiology of Mollusca edited by Wilbur and Yonge (1964, 1966) contains only few references t o them. The physiological studies carried out so far have been based on observations on very few species and are concerned chiefly with factors affecting settlement, reactions t o changes in certain physical and chemical features of the environment, digestion of cellulose, respiration, glycogen metabolism and the mechanism of boring. The chemical composition of a number of marine organisms has been studied and a comprehensive literature exists (see Vinagradov, 1953). For the Tcredinidae information is confined t o the observations of Lane et al. (1952) on the distribution of glycogen in Teredo (Lyrodus) pedicellata, of Lasker and Lane (1953) on the origin and distribution of nitrogen in T . bartschi and of Greenfield (1953) on the nitrogen and glycogen content of T . (Lyrodus)pedicellata. The importance of such studies lies in the fact that the gonad is the locus of intensive biochemical synthesis a t the time gametes are being formed (Giese, 1959). It is known that in the male large amounts of nucleic acids are needed for the sperm heads and in the female lipids and protein are mobilized to be stored in the eggs. These aspects have been studied by us (Saraswathy and Nair, 1969a) since we felt that Nausitora hedleyi with its peculiar restricted breeding habits can be expected t o undergo variations in its biochemical composition during the yearly cycle. This is all the more probable since the gonad may form about 45% or more of the entire wet weight of the animal during the breeding season, and may fall to as low a level as 2.97% during the non-breeding period. Annual reproductive cycle analyses were carried out in the hope that correlations might emerge to serve as a basis for a clearer interpretation of the annual reproductive cycle. In these biochemical studies detailed comparisons and generalizations are rather difficult owing t o the difference in the collection of material and in the methods adopted for estimation by the various authors. Our estimations have been made on entire animals collected from Cochin backwaters for a period of 12 months. All biochemical estimations were made on material dried t o constant weight. Water content, ash content, glycogen, protein, total nitrogen and non-protein nitrogen, lipids, calcium, phosphorus and chloride content were estimated. Glycogen estimation was done according t o the method of ))

TABLEIx. THE AVERAGE WET WEIOHT, GONAD INDEX, DRYWEIGHT, WATER CONTENT AND THE PERCENTAGE O F BODYCONSTITUENTS OF N. hedleyi DURING TEE DIFFERENT MONTHSOF THE YEARALONG WITH THE SALINITYOF THE AMBIENT WATER

Nov.

Dec.

Jan.

Feb.

March

April

May

June

July

Aug.

Sept.

Oct.

0.895 15.81 0.2 19 75.63 28.69 17.43

0.472 15.42 0.102 76.61 28.28 24.24

0.337 6.11 0.09 69.46 19.71 18.53

0.234 7.29 0.093 57.04 33.35 15.99

1.5 12.8 0.56 62.98 52.22 10.5

0.365 15.56 0.145 59.38 45.53 16.83

0.732 13.46 0.255 64.63 35.13 15.89

0.191 4.99 0.054 69.80 19.31 26.33

0.782 16.36 0.141 80.77 21-91 22.44

0.416 23.62 0.10 83.60 29.3 20.05

0.588 32.28 0.106 81.17 28.07 24.31

1.09 32-45 0-25 76.87 34.23 18-75

4.84

5.89

5.73

4.78

3.77

5.03

4.85

5.85

5.07

5.02

5.62

5.46

2.06 8.34

2.02 6.45

2.76 5.89

2.22 5.0

2.09 5.42

2.34 4.43

2.31 4.64

1.64 3.46

1.48 5.44

1.82 5.29

1.73 6-41

2.46 4.39

. .

7.31 8.61 0.62 7.1

4.49 7.1 0.86 12.08

9.45 10.87 1.37 12.59

4.57 7.05 0.97 13.77

3.16 5.31 0.62 11.58

4.71 8.04 1.04 12.9

4.86 7.25 1.12 12.2

2.30 11.45 1.39 12.15

0.39 4.68 1.02 21.74

0.39 6.71 1.51 22.48

0.37 5.44 1.09 19-99

1.01 5.05 0.49 9-79

0.50 7.0 23.23

0.51 4.7 32.48

0.56

.

0.49 5.63 17.36

8.0 32.94

0.54 10.29 33.36

0.83 10.27 33.63

0.54 9.82 33.38

0.56 1268 25.71

0.69 14.67 2.77

0.77 11.52 0.65

0.67 12.33 2.34

0.71 13.97 3.32

Constituents Wet weight in grams . Gonadindex . Dry weight in grams . Water content Glycogen in dry weight Protein in dry weight . Total nitrogen in dry weight . Non-protein nitrogen in dry weight . Lipids in dry weight Chloride content in dry weight (chloride as sodium chloride) Ash in dry weight Calcium in dry weight Calcium as yo of ash Phosphorus in dry weight . . Phosphorus as yo of ash Sa1inityp.p.t.

.

.

.

.

.

.

433

"HE BIOLOUY OF WOOD-BOmG TEREDINID MOLLUSCS

M a d e l and Hooglmd adopted by Raymont and Krishnaaw(tmy (1960) and expressed as percentage of glucose in dry tissue. For determination of the total nitrogen content, the conventional method of microkjeldahl distillation as outlined by Steyermark (1961) was followed and for lipids the Soxhlet apparatus was used. The method of A.O.A.C. (1960) was followed for the determination of salts, ash content, calcium and phosphorus. The consolidated data representing the average values calculated from several individual readings in the case of water content, S%.

I-

% VaCl

% H2U

F I ~42. . Curve8 showing the average salinity of the ambient water: (A) monthly d ations in the percentage of water content ;(B)and sodium ahloride (C) in the body of Nazcsitora hedleyyk.

434

N. BALAERISJ3NAN NAIR AND M. SARASWATHY

glycogen, proteins, total nitrogen and non-protein nitrogen as well as estimations of pooled monthly samples for lipid, sodium chloride, ash, calcium and phosphorus are presented in Table IX. Average monthly salinity and the average monthly gonad index are also presented. The water content varied from 57.04-83-60%, with an average from specimens of varying sizes collected throughout the year of 71.49% for this species. For marine species of Teredo, Lasker and Lane (1953) found the water content to be 73% at Biscayne Bay, Florida. The relatively low values obtained appear unique among the Bivalvia (see Vinagradov, 1953)and are probably due t o the peculiar habitat, indicative possibly of the stress of high salinity on the life and activity of this shipworm. The influence of salinity on the water content of N . hedleyi is shown in Fig. 42. Venkataraman and Chari (1951) and Durve and Bd (1961) have reported a reciprocal relationship between water content and such organic constituents as fat, glycogen and protein in oysters. A n inverse relationship between the water content of the body and the salinity of the ambient water was evident. It was also observed that the water content in females was higher than in males and that the range of fluctuation was more conspicuous in the former. Glycogen is an important food reserve of many marine molluscs being needed for reproduction, growth and maintenance. Glycogen values were notably high during the non-breeding months especially during February to May when they fluctuated between 33-35 and 52.22% of the dry weight of the animal. From June to January the values were comparatively low. On the onset of the breeding season there was a perceivable fall in the glycogen content, probably owing to the initial mas8 spawning during June. After January the values were comparatively high and reached the highest value for the year in March. Some animals bore into timber for protection only but shipworms digest and metabolize the cellulose of the wood into which they bore and exploit it as a source of nourishment. This unusual ability is attended with several morphological and physiological adaptations associated with the new conditions of habitat and food involving changes in metabolism necessitated by a diet that is chiefly carbohydrate (Dore and Miller, 1923;Boynton and Miller, 1927 ; Lane, 1955; Nair, 195513, 1955~) 1956c, 1957b). The concentration of glycogen which is even higher than that present in very " fat )' oysters has already been reported by Lane et al. (1952) who report as high a value as 58.2%. Greenfield (1953) has shown that glycogen constitutes 30% of the dry weight of Teredo. Scrutiny of individual values in our studies shows that glycogen value in some specimens may reach 59.12% in

435

THE BIOLOGY OF WOOD-RORINQ TEREDINID MO1,LUSCS

terms of dry weight of the body in Nausitom hedleyi. This is probably the highest value recorded for any mollusc. Whet'her this apparently higher value is associated with thc peculiar esbuarinc habitat and the restricted nature of its breeding or with any other physiological peculiarity is, however, not evident.

1 mq

9:. I

24

-

20

-

16I2

N

D

J

F

rd

A

M

J

J

A

s

o

Fra. 43. Curves illustrating the average dry weight of the specimens in respcctive months (A) together with the monthly variations in the percenhgc of glycogen, (€3) and protein, (C) content of the body of Nnusitora hedleyi.

Correlation between glycogen values and the breeding period is evident in the present study. Such seasonal changes and high values for glycogen during the non-breeding resting phase have also been noticed in oysters (Okasaki and Kobayashi, 1928 ; Tully, 1934 ; Durve and Bal, 1961). Greenfield (1953) was unable t o notice any seasonal change in the nitrogen and glycogen content or any apparent difference in the concentration of these components between gravid and nongravid individuals of the same size. It may also be seen from the A.P.B.-9

I5

430

N . BALAKRISHNAN NAIR AND M . SARASWATHY

present study that glycogen in N . hedleyi not only changes seasonally, but also between gravid and non-gravid individuals. It seems probable that glycogen, though a storage material in both sexes, is rapidly used up in the female for the formation of ovocytes. It was interesting to note that the minimum concentration of glycogen is in females at the end of the breeding season. Contrary t o the results obtained by Sreenivasan (1963a) in Martesia fragilis, the glycogen content is, on an average, higher in males than in either the indeterminate forms or in the females. However, a similar result with comparatively high values of glycpgen has also been obtained from the shrunken, spent male gonad of the chitons Katherina tunicata (Giese and Araki, 1962) and Cryptochiton stelleri (Tucker and Giese, 1962). Generalization is, however, difficult owing t o the paucity of information since Lane et al. (1952) do not give any data with reference to sex and maturity. An increase in glycogen content is also evident with an increase in weight. A similar observation has also been reported for the Miami species by Lane et al. (1952) and Greenfield (1953). Detailed histochemical studies may throw further light on the distribution of glycogen. Lane et al. ( 1952) have reported considerable concentration of glycogen in the muscles and also in the gill and in the imbedded larvae. I n the pholad, Martesia striata Nagabhushanam ( 196la) estimated that glycogen forms about 3% on the basis of dry weight of adult specimens. This was chiefly concentrated in the gonad and the muscles. A decrease of about 62% was noted in animals kept in plankton-free sea water for 10 days. He found no seasonal variation of glycogen in this borer. I n N . hedleyi the protein content was generally high from June t o January. The total nitrogen values were apparently steady both during breeding and non-breeding periods. The values for non-protein nitrogen indicate that in general this was poor during a major part of the breeding season. It has been reported (Lasker and Lane, 1953; Greenfield, 1953) that the nitrogen content of adult Teredo is generally very low and this has been attributed to a dominant cellulose diet. This generalization seems t o be justified and our studies indicate that the values for total nitrogen are generally low. However, it may be noted that in Nausitora hedleyi, though the total nitrogen content (5.16) is higher than that in Teredo pedicellata (2.17), it is much less than in other molluscs such as Martesia fragilis (Sreenivasan, 1963b) in which a value as high as 11.7 has been recorded. The higher nitrogen content noticed in this species is perhaps due t o its habitat in highly productive estuarine areas. The greater amounts in smaller specimens of this species has been noticed in Teredo pedicellata also (Greenfield, 1953). Similarly in both Martesia striata and M . fragilis the unit nitrogen con-

THE BlOLOCY O F WOOD-BORING TEltYUINIU MOLLUSCS

437

tent shows a slight but gradual decrease with increase in body weight (Sreenivasan, 1961). In Nausitora hedleyi the non-protein nitrogen content varies during the different times of the year. The difference is marked during the period June-October when low values prevail. Giese and Araki (1962) detected the presence of a surprisingly high percentage of non-protein

FIG.44. Curves showing the variat,ions in glycogen (A), and protein (B), content of Nausitora hedleyi in relation to increase in weight of the body.

nitrogen in the mantle of Katherina and the large amount of nonprotein nitrogen present in the testes was attributed to accumulation of nucleic acid in the sperm. They noticed no change in the non-protein nitrogen content in these chitons during the breeding cycle. I n the light of these observations, the following explanation for the fall in nonprotein nitrogen during the breeding season of Nausitora hedleyi may be given. During the non-breeding season, the non-protein nitrogen

438

N. BALAKRISHNAN NAIR

AND M. SARASWATHY

may be stored in the mantle which accounts for the comparatively high values during that time. On the onset of breeding season the stored reserves may be utilized for sperm formation. The only explanation, therefore, for its apparent fall on the onset of breeding season is the loss of this material through spawning. However, a clear picture of these cycles can be obtained only through a detailed analysis of the different organs separately. To find the relationship in N . hedleyi of glycogen, protein and total nitrogen content t o dry weight, specimens were grouped with a weight difference of 50 mg irrespective of sex, time of collection or length. The average glycogen content of animals below 50 mg was about 23.17% and the values showed a steady increase t o reach more than 50% of the weight of the animal, in specimens above 400 mg. I n this estuarine species glycogen in terms of per cent dry weight is higher than in other wood borers such as Teredo pedicellata and Martesia striata or in oysters. The protein content of animals in the weight group 0-50 mg was found t o be the highest (23.51%) and this constituent continued to be high (18%) even in specimens of the weight group 250-300 mg. But in higher weight groups the protein content was found t o be very low ( 10.5y0) indicating an inverse relationship between glycogen and protein content. The total nitrogen content had a similar trend to that of protein with high values in smaller animals. The lipid content expressed in terms of percentage of dry weight varied from 3.46 in June t o 8.34 in November and was low during April and May. Correlation between lipid content and breeding period was not evident. I n N . hedleyi lipids constitute only a small percentage of the dry weight, unlike chitons (Giese and Araki, 1962) where this reaches levels of 29% in some organs. A marked seasonal variation in the fat content was not noticed in Martesia striata (Nagabhushanam, 1961). The lipid content does not significantly vary throughout the year. Glycogen is the most important storage material in N . hedleyi. The percentage of salts (chloride as sodium chloride) expressed as percentage of dry tissues showed a distinct fall on the onset of the breeding season which in this case coincided with a fall in salinity. During the highly saline period of February, March and April the salt content of the body was curiously low. The ash content expressed as percentage of dry weight varied from 11.45 in June t o 4.68 in July, i.e. there is a noticeable fall of the ash content soon after the onset of breeding. On average the amount of ash in this species is about 8.12% of the dry tissue, thus falling within the usual range in mature molluscs. The calcium content (Fig. 45) of the species expressed as percentage of the ash content fluctuated between 7.1 in November and 22-48 in August.

THE BIOLOQY O F WOOD-BORING TEREDINID MOLLUSCS

439

The values were comparatively high during July, August and September and were low during October and November. A similar trend was noticed in respect of the phosphorus content although the amount present seems to be much less than of calcium. The data regarding the mineral constituents give the impression that coinciding with the period of spawning and the consequent loss of

F ~ Q45. . Curves illustrating the monthly variations in the calcium (A), and the phosphorus (B), content of Nausitora hedleyi expressed as percentage of ash content of the body. Curves (C) and (D)represent the calcium and phosphorus content respectively expressed as percentage of dry weight.

weight owing to a fall in the organic constituents, there is an apparent increase in the calcium content of the body, as reported for oysters (Durve and Bal, 1961). From the above study of the variations in the chemical composition of N . hedleyi it appears that there are two periods of variation, the first from June to December coinciding with breeding activity and the other from January t o May representing a period of rest. In the first period the values for water content, protein, total

440

N. BALAKRISHNAN NAIR AND M. SARASWATTHY

nitrogen and in general for calcium and phosphorus are high while in the second period glycogen and non-protein nitrogen show an increase with an apparent fall in the percentage of the constituents which showed higher values during the first period. Respiration in both larval and adult teredinids has been investigated (Lane and Tierney, 1951 ; Lane and Greenfield, 1952). The oxygen consumption of the larva (Fig. 46) reaches its maximum at 24 h (normal free-swimming period 72 h) and decreases gradually until death occurs at about the tenth day if it has not succeeded in penetrating wood. These high values have been attributed to increased ciliary activity.

Age in days

FIG.46. Curve of normal respiration of unattached Teredo larvae and of the observed incidence of crawling in a series of laboratory cultures. Larvae that do not crawl progress by swimming. (After Lane, 1965.)

Measurements of the oxygen uptake show that through the entire freeliving larval life the average value, at 25"C, is about 25 pl oxygen per hour (Lane, Tierney and Hennacy, 1954). The oxygen consumption of the adult varies widely, being generally higher in animals in the wood than in those removed from it. The rate curves indicated cyclic variations suggesting the existence of a poorly developed or relatively ineecient respiratory control mechanism. Small specimens showed a higher oxygen consumption than larger ones. The magnitude of the respiratory stream has also been studied (Lane and Gifford, 1954). Under normal conditions the average rate of ventilation was found to be 4.1 I. of water per hour per gram of dry weight of the animal. This circulation is maintained by the cilia of the gills and the visceral mass. The general mantle circulation is also assisted by the peristaltic movements of the inhalant siphon.

THE BIOLOGY OF WOOD-BORIXO TEREDINID MOLLUSCS

44 1

XVI. FOOD AND DIGESTION All wood fragments scraped off during drilling pass through the alimentary canal which has been greatly specialized with special pouches like the caecum (appendix) for the reception of wood and the specialized region of the digestive diverticula for the intracellular digestion of cellulose. Potts (1923) observing the ingestion of wood fragments by the " liver " cells of Teredo suggested the possible direct utilization of wood in the nutrition of the animal. Various authors have suggested that the excavated wood is used as food. Harrington (1921) was perhaps the first to present experimental proof that the extracts of the digestive diverticula of Teredo norvegica could break down cellulose. Dore and Miller (1923) and later Miller (1925) demonstrated that about 80% of cellulose and 1 5 4 6 % of hemi-celluloses disappear from the wood during its passage through the digestive tract of T. navalis. Lazier (1924) gave some evidence on digestion of wood particles by scrutinizing the staining reaction with haematoxylin of cellulose in different regions of the digestive tract. Hashimoto and Onoma (1949) showed the presence of cellulase, alginase and xylanase activity in the " liver " of Teredo while Mawatari (1950) identified amylase, cellulase, cellobiase, saccharase and maltase in the midgut. Miller and Boynton (1926) analysed samples of wood particles taken from the caecum of B a n k i a setacea, and found the percentage of reducing sugars to be as high as 3.86 while in the wood it was only 0.92. Boynton and Miller (1927) analysed various parts of the digestive tract and demonstrated the presence of cellulase in the digestive diverticula and its absence in the crystalline style. Miller and Norris (1940) later confirmed that extracts of the digestive diverticula contain cellulase and further showed the presence of amylase, phosphatase, lipase, catalase, peroxidase urease and a tryptic-type proteolytic enzyme. The style contained only amylase according to these authors. Lane and Greenfield (1952) have reported the presence of a cellulase enzyme system located in the general gut wall " in the anterior third of the gut " of Teredo. Greenfield ( 1955) separated and concentrated this cellulase from tissue homogenates by adsorbing it on cellulose gum and later recovering the enzyme by ammonium sulphate precipitation. Greenfield andLane (1953)also demonstrated that cellulase activity in that part of the alimentary canal which includes the caecum, the intestine and the rectum is approximately double that in the region anterior to the caecum. Nevertheless, Zobell (1946) pointed out that the question is still open whether the cellulases and lignases present in the digestive tract of Teredo are produced by the animal itself or by commensal

442

N. BALAKRISHNAN NALR AND M. SARASWATHY

bacteria. The bacteria themselves, the author suggests, may serve as food. Bacteria play a role in the softening of submerged wood surfaces which may make the wood more susceptible to attack by marine borers. That cellulose is broken down by bacteria and not by enzymes has also been suggested by Johnson (1949),while Deschamps (1953) questioned the presence of an enzyme produced by the animal since he could not distinguish the cellulase of bacterial origin from that produced by the animal. Nair (1955b, 1955c, 1956c, 1957b) investigated the nature and properties of the enzymes in the style and the digestive diverticula of Bankia indica. Wood particles are found in the caecum in a highly disintegrated state along with reducing sugars. It was, therefore, inferred that the style may contain a cellulase. A suspension of regenerated cellulose was incubated with the enzyme extract and the change in turbidity was measured colorimetrically (Nair, 1955~). A marked decline in turbidity was observed in experimental tubes. This test was confirmed by determining the cellulose left undigested. The extent of digestion of cellulose was also verified by determining the sugars formed in the reaction mixture according to the method of Somogyi (1930). The amount of sugars formed at the end of the different incubation periods were also estimated. The path of cellulose degradation was studied by chromatographing the hydrolysates and determining qualitatively the end products of cellulase activity. Enzyme preparations from the digestive diverticula and from the style were used. The substrate was either sawdust or regenerated filter paper. The digestive mixtures were incubated at 30°C for 5 days and the hydrolysates analysed at intervals. Rf values indicated the presence of cellobiose and glucose in the active preparations, The hydrolysates from the style showed the presence of both cellobiose and glucose at all stages of hydrolysis (Nair, 1956e). From this it was presumed that the style enzymes by themselves are incapable of hydrolysing cellulose completely into glucose and that part of the cellobiose is apparently hydrolysed later at some other site in the digestive tract. The extract of the style of Bankia was found to be capable of hydrolysing glycogen and also showed some activity on lactose and maltose (Nair, 1957b). The stomach contents of Bankia have an average pH of 5.8 due to the dissolution of the style which has a pH of 5.5. The optimum pH for the activity of the enzymes of the style (pH 5.9) is about the same as that of the stomach where these are active. The optimum duration of hydrolysis is 5 h and the optimum temperature 31OC. The enzyme system gets inactivated by heating for 15 min at 60°C. The enzymes of the digestive diverticula comprise an effective carbohydrase enzyme

THE BIOLOGY O F WOOD-BORING TEREDINID MOLLUSCS

443

system capable of digesting starch, sucrose, glycogen, maltose and lactose, cellulose in wood, regenerated filter paper, cellobiose and gum arabic, and also comparatively weak proteolytic and lipolytic enzymes (Nair, 1956~).This weak protease activity in Bankia is in conformity with the observation that the nitrogen content of adult shipworms is low (Greenfield, 1953). Thus, the amount and nature of the enzymes produced by the digestive diverticula probably depend more or less on the natural diet and on the amount of food available. There does not seem to be any appreciable difference in enzyme equipment between species having different diets. There appears to be no exclusion of certain enzymes in relation to food specialization in the Bivalvia. Most animals are incapable of digesting cellulose because they lack the necessary enzyme equipment but shipworms which chiefly live on wood are an exception possessing a strong carbohydrase system in the crystalline style and the digestive diverticula. The capacity to elaborate cellulase, cellobiase and enzymes capable of hydrolysing pentosans in addition to the carbohydrase enzymes is as much an adaptation to their peculiar diet as the modification of the alimentary canal, the shell or the foot. This fact is obvious when we find that the capacity of other bivalves to split not only carbohydrates but also proteins and fats is retained by B . indica. Closely correlated with this emphasis on the digestion of carbohydrates is the capacity for the storage of great quantities of glycogen (Lane, Posner and Greenfield, 1952 ; Greenfield, 1953; Lane, 1955; Saraswathy and Nair, 1969a). The conclusions of Johnson et al. (1936)and Bartsch (1922)that the shipworm can live on plankton alone even after all the available wood is exhausted appear to contradict the findings of Potts (1923), Roch (1932), Lane (1955) and Becker (1959)that the supply of wood is the principal food constituent. Since shipworms are equipped with all three sets of digestive enzymes, they must be capable of living not only on wood but also on other items of food both living and non-living brought into the body along with the respiratory current of water. Conclusive tests based on the exclusion of all water-borne materials are difficult. Even under normal conditions shipworms may not be living on wood alone but also on plankton (see Fig. 47), as shown by Dore and Miller (1923) for Teredo navalis, Lasker and Lane (1953) for Teredo and Quayle (1959) for Bankia setacea. However, it is not improbable that other factors such as the high specialization in the sorting mechanisms which permit only a small quantity of very small particles such a s the nanoplankton to enter the gut, the major part being rejected as pseudofaeces might be one cause for their reported mortality after the wood supply is exhausted. Becker (1959)was able to rear Lyrodus pedicellatus through four generations in

444

N.

BALARRISHNAN NAIR AND M. SARASWATHY

artificial sea water without any additional food but was not successful with Teredo navalis since they failed to breed, probably on account of the inadequate nutrition, owing to the absence of any protein-rich plankton. It is probable, as Turner (1966) has suggested, that “ the adults of some species may require planktonic food at least during the breeding period and some may be capable of surviving on plankton only as do many other bivalves ”. Probably this is true of Kuphws, Teredora and Uperotus. Plankton with its rich nitrogen content must be essential for the normal growth of shipworms. This conclusion has been confirmed by the recent experiments of Karande et al. (1968) on Teredo furcifera which were maintained in aquaria from initial settlement ;they grew and propagated only if they were provided with nanoplankton through a system of running sea water. These authors maintained these borers in laboratory tanks over a period of 2 years raising 0

0

0 leucine

phenylalanine

0 0

0 valine

0

0 tyrosine

0

0 proline

rnethionine

0

0

0

0

alanine

0

0

arginine

Teredo Wood Nanoplankton

FIG.47. Amino acid composition of adult Teredo, of the wood in which it lives and of nanoplankton collected from local s m water. (After Lane, 1955).

five generations under controlled conditions. These observations are significant since wood has been shown to be deficient in the aromatic amino acids phenylalanine and tyrosine, in the heterocyclic amino acid proline, and in valine, all of which are present in shipworms. Hydrolysates of nanoplankton contain all of these missing amino acids except phenylalanine (Fig. 47). There is also the factor of overcrowding which turns the timber into a porous and highly fragile mass permitting entry of parasitic Protozoa and harmful bacteria-a serious menace to the life of the community as found by Grave (1928). Probably it is under these conditions that shipworms perish owing to the depletion of the substrate and not because of starvation. The observation of Lane (1955),that “population

THE BIOLOGY O F WOOD-BORING TEREDINID MOLLUSCS

445

density influences the duration of adult life more than any other single factor ” is significant. The conversion of cellulose into assimilable sugars seems to be accomplished by enzymes both from the style and the digestive diverticula. The role of the former is probably preparatory, acting on large molecules and reducing the food into a soluble state, enabling extracellular digestion of the non-nitrogenous food to take place in the stomach and the caecum (appendix) especially the large wood fibres which cannot be taken whole into the cells of the specialized region of the digestive diverticula (Nair, 1955b, 1955c, 1 9 5 6 ~ )1957b). It is evident that the style splits the cellulose into the intermediary cellobiose and probably passes it on for intracellular digestion in the diverticula (Nair, 1956e). It is not known whether this disaccharide, cellobiose, can be directly absorbed by the coiled typhlosole of the caecum. Thus the cellulose splitting seems t o take place in steps in two different sites, one extracellularly in the caecum and the other intracellularly in the vacuoles of the digestive diverticula which has a cellobiase powerful enough to complete digestion, thereby fully exploiting the nutrient resources of the wood. Phagocytes playing an important role in the digestive process are not, however, improbable, for Yonge (192(1, 1926a)has noticed phagocytes around the stomach, digestive diverticula and midgut passing into the lumen of the gut ingesting particles of food which they later carry back to the tissues and digest. Phagocytosis does occur in the digestive diverticula of Mytilus, Ostrea (Vonk, 1924) and Teredo (Potts, 1923). Greenfield (1959), who summarized previous work, concluded that the evidence from experimental data strongly suggests cellulolytic activity in shipworms and the utilization of the end products of the process. It will also be worth while, as suggested by Turner (1966), to “ investigate the presence of bacteria and fungi in the wood itself and check on the possible reduction of the cellulose before it is ingested by the shipworm.” Despite this evidence strongly in favour of enzymic hydrolysis of cellulose, Florkin and Lazet (1949) showed that in the classical case of HeEix pomatia cellulase is produced by (symbiotic?)bacteria. Jeuniaux (1950, 1954)investigated the origin of chitinase and found that bacteria produce this enzyme and not the snails (Achatina fulica, Helix nsmoralis, H . aspera, Limax cinereoniger, etc.). Therefore, as Wee1 (1961) has cautioned “ future investigations on species believed to produce special enzymes themselves will be needed to show whether this claim is correct or not.” It will also be interesting to find out the effect of ageing on the production and utilization of enzymes in these specialized bivalves.

446

N.

BALAKRISHNAN NAIR AND M. SARASWATHY

Recent biochemical studies (Liu and Townsley, 1968) on the digestive metabolism of cellulose and its derivatives in the caecum of Bankia setacea have demonstrated the presence of Embden-Meyerhoff pathway, the pentose cycle, and the citric acid cycle as well as the non-trioare pathway. Not less than twenty-five enzymes including several Key enzymes have been identified in the above mentioned pathway. These authors could not notice the presence of any cellulolytic bacteria in the caecum of the shipworm. Liu and Walden (1969) have also developed a quantitative spectrophotometric assay for cellobiase. XVII. ECOLOGY There are several environmental factors which affect the natural populations of shipworms. These are the physico-chemical variables of sea water, such as temperature, salinity, oxygen tension, turbidity and pollutants ; the presence and intensity of fouling organisms ; the nature of the wood, depending on the species of timber, its softness and orientation of the grain ; the length of exposure of the wood sample in water ; the presence or absence or the nature of the preservatives used on it ; the location of the wood in relation to tidal changes, whether or not it is periodically exposed to desiccation; the orientation of the sample in relation to depth ; nature of the bottom ; mechanical effects of currents, their velocity ; conditions of illumination ; the interaction of the species of wood-boring animals present in the area ; the availability of a suitable substrate during settlement ; the effectiveness of local larval sources in the case of shipworms and the presence or absence of predators and parasites. The occurrence, abundance, and so the intensity of attack, in any locality is dependent on these factors which vary widely from year to year. Probably there are several more, but these factors are the most important. Variations in the borer populations from year to year in any locality are no doubt due to a very involved association of these factors, some of which occasionally stand out as the most responsible ones while other factors, none attaining conspicuous importance by itself, may collectively exert as much or more influence than more prominent and easily followed factors. It is by a constant shifting of importance of these factors and new alignments in their association owing t o ever varying conditions, that accounts for variations in local abundance of shipworms. This would explain periodically recurring devastations separated by often lengthy intervals of comparative freedom from attack (Vrolik et al., 1860; Harting, 1862; Dons, 1949; Scheltema and Truitt, 1954). Reasons for increased attacks have not all been investigated but they may be different in different localities such as lowered salinity (Sellius, 1733)

THE BIOLOGY OF WOOD-BORING TEREDINID MOLLUSCS

447

caused by reduced inflow of fresh water or reduced rainfall causing an increase in salinity (Baumhauer, 1860; Vrolik et al., 1860; Harting, 1862), high temperature and dry summers (Hoeven, 1861) or an unusual increase in water temperature (Dons, 1940, 1949).

A. The inJluence of temperature on the activity and distribution of shipworms Temperature is a major influence on the activities and distribution of shipworms and is a limiting factor in growth, reproduction and distribution. There is a complex correlation between the biological effects of temperature and salinity, the former can modify the effects of the latter and change the salinity range of an organism (Kinne, 1963). The temperature cycle is a mere reflection of the annual fluctuation in mlar radiation and this factor affects animals in other ways as well, such as influencing photosynthesis of the phytoplankton. Temperature also influences precipitation, thereby affecting salinity. Species living in different geographical locations are adapted to different ranges of temperature and each species usually has an optimum temperature. There are maximum and minimum temperatures as well. Lethal extremes vary greatly from species to species. Temperatures that are too low for some species may be favourable or tolerable for others. The minimum, optimum and maximum temperatures all vary with species and even that of the same may change through periods of acclimatization. These enable different species to establish themselves in every available life zone. Some species are characteristically restricted to the cold waters of higher latitudes, others are typically inhabitants of subtropical areas while a majority are denizens of the tropical regions illustrating the general rule that tropical biotopes are typically rich in species. Thus along the coasts of Norway 3 species of shipworms occur (Nair, 1959), 5 species in the Mediterranean, 7 species from Hawaii and Midway Islands, 16 species from the Philippine Islands (see Turner, 1966) and 22 species from the east and west coasts of India (Nair, 1968). Limiting winter temperatures and minimal summer heat determine boundaries of distribution towards higher latitudes. Limiting maximal temperatures for survival occur in summer and minimal temperatures for reproduction and growth in winter, these determining the boundaries of distribution towards the equator. Uniformly high tropical temperatures hasten metabolic activities and accelerate growth rates, leading to the attainment of sexual maturity at a surprisingly early age. Some species breed almost continuously and several generations are produced, in rapid succession within a single year. The speeding up of life histories favours the acceleration of the evolutionary

448

N. BALAKRISHNAN NAIR AND M. SARASWATHY

process. This has often been cited as the reason why the tropical zone is richer in genera and in species than elsewhere. The existence of numerous species along tropical coasts poses a serious problem regarding specific identification and accurate assessment of the destruction each species inflicts. The majority of the known species of shipworms are active and breed during the warmer months of the year (Kindle, 1918, M'Gonigle, 1926 ; Mackenzie, 1927 ; Nelson, 1928 ; Cheney and Searles, 1935; Zvorykin, 1941 ; Tarasov, 1943; Dons, 1945, 1949; Mawatari, 1950; Nagabhushanam, 1962). This is particularly conspicuous in the higher latitudes where the seasons are well marked with wide temperature variations. Here during the late spring and early summer, the temperature rises above the threshold and remains above that value sufficiently to allow active growth and reproduction. For the developmental and larval stages to survive, the water must be sufficiently warm. Therefore, the parent is stimulated t o expel the gametes or the larvae when the temperature of the water reaches a specific point for each species. In the Adriatic, Teredo navalis, T . utriculus (larviparous) and Bankia minima are summer breeders, Teredo pedicellata is a winter breeder when the female phase occurs in T. utriculus (Roch, 1940). However, there are such species as T . norvegica (Nair, 1959, 1962) which can breed during the cold months of the year. I n higher latitudes a slight increase in the normal summer temperatures may lead to an increase in activity (Cheney and Searles, 1935; Clapp, 1935 ; Tarasov, 1943 ; Riabchikov, 1957). Similarly a perceivable retardation of their activity occurs during unusually long and severe winters (Anon., 1943a) which may even completely destroy these pests in certain areas (Smollett, 1790). Extremes of heat or cold may completely wipe out entire populations at whatever season the most vulnerable stage of development occurs (Anon, 1943a). Shipworm attacks are not necessarily annual ; they are periodically recurring phenomena. One among the several reasons for this especially in higher latitudes is temperature. Adult shipworms are known to survive wide variations of temperature and salinity (Anon, 1927 ; Chenney and Searles, 1935). This enables them to be transported through wide areas where they are likely to experience without serious ill effects temperatures either above or below the optimum for the species. For T. navalis of the Atlantic coast of Canada 22-5OC appears the optimum and a temperature of 7.5"C is unfavourable (Anon, 1927). At Kristineberg (Sweden), T. navalis is most active in the temperature range between 15-25OC and can tolerate temperatures from 5 to 30°C. It can even survive for some

THE BIOLOGY O F WOOD-BORING TEREDINID MOLLUSCS

449

time at the freezing temperature of sea water (-1.4"C) (Roch, 1932). In the Black Sea the most suitable temperature for Teredo sp. is between 15-25°C (Zvorykin, 1941). Here a temperature of - 1°C is lethal, at f l to +5"C the animal is moderately active and above 25°C there is a decline in activity and death occurs at 30 to 38°C. At low temperatures animals may survive 24 days in wood taken out of water (Zvorykin, 1941). I n Japan (Mawatari, 1950) the lethal limit for teredinids has been fixed around 8-10°C. For T . navalis Imai et al. (1850) noted that boring ceased at temperatures below 14OC or above 26°C. I n the comparative warm waters of Hawaii both adult and larval shipworms survived 35°C for hours. Cooling from 8 to 0°C caused inactivity but recovery followed when brought back to normal ternperature (Edmondson, 1942). Thus shipworms are generally most active between 15-30°C. The optimum temperature may be considered that value at which a certain process goes on fastest. But the temperature for the maximum rate often varies considerably for different processes within the same organism and also for the same process at different stages in the life cycle. The optima for the various developmental stages are, however, different from the optimum for the adult. This is a particularly important factor in the case of the shipworms because the free-swimming larvae are the infective stage. The uniformly high temperature of the tropics can stimulate sexual activity, accelerate development of the gonad, hasten maturity and shorten the free-swimming larval period. These contribute towards the production of several spawnings in a single year leading to an almost continuous settlement of waves of borers which bring about speedy destruction of timber. Growth has been considered as the consequence of assimilated food not diverted to other purposes such as respiration or muscular activity (Moore, 1966). Loosanoff and Nomejko (1949) have demonstrated a relationship between the growth rate of Ostrea virqinica and temperature, there being an optimum temperature above and below which growth decreases. There are cases on record of geographical variation in size in which temperature is apparently a controlling factor. Nevertheless, it is not clear whether the regions characterized by the larger sizes are areas of rapid growth or of long continued slow growth. There is indeed, a general impression that larger forms tend to be found in colder waters. As early as 1860, Jeffreys noted that specimens, probably of Teredo meqotara, from Greenland were twice the size of those found along the British shores and T.philippi was found to be larger round the British coasts than in southern localities. He also observed that T . norveqica,

450

N. BALAKRISHNAN NAIK. AND M. YARASWATHY

T . navalis and T . pedicellata of the British Isles exceeded in size those found along the coast of Spain and Sicily. Sigerfoos (1896) states that Xylotrya Jimbriata (= Bankia gouldi Bartsch) a t Beaufort, N. Carolina grew t o a length of 100 mm in 36 days. Orton (1914) found Teredo nccvalis growing t o a length of 19.8 cm in 31 weeks. Potts (1921) made preliminary observations on the comparative growth rates of certain marine organisms of temperate and tropical seas and noted a faster growth rate for Teredo from the tropics. Nair (1962) noted that there was a retardation in the growth of T . megotara in western Norway with the onset of cold conditions. For this species Kramp (1927)’ noted at Hirtshals, a growth of 15 cm in 6 months and 26 cm in 1 year. Nair (1962) obtained a maximum length of 28.6 cm for a period of about 5 months for this species a t Espegrend, W. Norway while Dons (1940) observed at Trondheim, one of 37 cm in 6 months and of 52 cm in 1 year. Needler and Needler (1940) noted a correlation between maximum growth rates in shipworms and highest temperature. Even though in the warm tropical waters Nair (1960) was not able t o notice any correlation between growth rates and hydrographic conditions for Bankia indica (=B. carinutu) a t Madras, Nagabhushanam (1961) was able to record maximum growth for Teredo furcillatus (=T. furcifera) in May coinciding with the highest temperature for the year at Visakhapatanam. Studies by Potts (1921) on Teredo sp. showed that this attained sexual maturity and produced larvae in 24 days and in less than 1 month infected wood was riddled by its burrows. I n many shipworms, the spawning activity is stimulated by rising temperature. Thus Nelson (1928) has shown that T . nawalis spawns when the temperature reaches 15-16°C and this spawning temperature has been cited as a factor which has facilitated the spread of this species to most parts of the world. I n Onagawa Bay, Japan, according t o Imai et al. (1950) it spawns from early summer (temp. 18°C) to late fall. T . navalis at Milford were conditioned t o spawn by Loosanoff and Davis (1963) in sea water maintained a t a temperature between 15-20°C. Spawning occurred a t temperatures of 14°C and higher, and larvae were released a t temperatures ranging from about 16-20°C. Grave ( 1 928) reported that this species spawned when the water temperature reached 11-12°C. Imai et al. (1950) found that spawning begins when the water temperature reaches 18°C. Sullivan’s data (1948) closely agree with those of Loosanoff and Davis ( 1 963), spawning occurring a t approximately 15°C. At Ladysmith harbour, British Columbia, Ba.rLkia sdacea spawns when the water temperature reaches 10°C (Quayle, 1959a), and at Puget Sound for the same species between 7-12OC (Johnson and Miller,

THE BIOLOGY OF WOOD-BORING TEREDINID MOLLUSCS

451

1935). Thus in shipworms, as in oysters (see Stauber, 1950) local physiological races may exist in which the spawning temperature, dthough relatively constant at any given place, may differ markedly dong different parts of the coast. The allied species B. gouldi in Chesapeake Bay, Maryland, spawns only when the water temperature is btween 16-20°C (Scheltema and Truitt, 1954). Long spawning seasons may be due to various causes. If a species lives over a considerable vertical range, then the critical temperature for spawning will be reached at different dates at different depths (Thorson, 1946), different age groups may spawn at different times or srtch individual may spawn for short periods over the whole breeding season and if this is rhythmical, it may result in a continuous production of young ones over a long period (see Fretter and Graham, 1964). Within the range, growth rate is usually accelerated at higher temperatures. Thus in species from temperate waters such as B. setacea (Quayle, 1953)and B.gouldi (Sigerfoos, 1908)the free swimming veliger $age lasts for 3-4 weeks while in tropical forms such as B. indica (= B. mrinata) it is only about 17 days (Nair, 1956a). However, a low tempersture, if not lethal, may prolong the pelagic life of the larva and this may indirectly help it to find a piece of timber on which to settle and metrimorphose and also facilitate wider dispersal of the larvae under the influence of currents. But this extension of pelagic life also increases the period during which the larvae are exposed to predation (Thorson, 1950). According to Imai et al. (1950)the duration of the larval period of Teredo navalis in Onagawa Bay, Japan, is from 22 days to 1 month, the shorter period corresponding to the higher temperatures. The most sitive stage of shipworms is the embryo (6oth-8oth h) about the time of shell formation (Anon., 1927; Cheney and Searles, 1935; Zvorykin, 1941). Quayle (1956) reports that during summer the larvae of Bankia setacea occur at deeper levels than in the winter, apparently a reflection of temperature preference. It has been claimed that the distribution of shipworms has been effected to a larger extent through the passive dispersal of these within driftwood (Moll, 1941a), floating seeds (Moll, 1936), wooden hulls of boats (Kofoid et al., 1927 ; Brown, 1935), sea-water tanks of ships and log booms (Kirkbride, 1922). Brown (1816) states that tropical species have been carried to temperate or even polar regions. As a matter of fact such dispersal has not been so widespread and extensive as the claims indicate. The fact is that many tropical species have not been able to establish themselves when transported by such agencies to areas where the environmental conditions are not favourable (;Teffreys,

452

N. BALAKRISHNAN NAIR AND M. SARASWATHY

1861 ; Bartsch, 1922, 1931). For the permanent life of a species in an area, the prevailing temperature must never be so high or so low at any time 8s to kill the organism and the temperature must be suitable for a sufficient period to permit the reproduction, larval development and growth to sexual maturity of the species. The limitation in the geographical range is brought about by the most susceptible stage and the boundary of distribution is determined by the weakest link in the life cycle with respect to temperature tolerance. Other life stages may sometimes extend temporarily beyond the area of permanent cxistence. Osler ( 1 826) noted that though nearly 4 000 vessels arrived at Swansea annually shipworms had not been seen for years. It is probable that those brought from warmer areas are destroyed by the low winter temperatures. I n those instances where the adults with their comparatively greater powers of endurance are transported to areas where conditions are not very satisfactory, the adult animal may live at least vegetatively for some time though not capable of sexual maturity and spawning. Thus the absence of sufficient warmth for the susceptible early stages of development prevents the establishment of a native breeding population despite the fact that adults may be met with in the hulls of boats that visit the port or in the drift material cast ashore.

B. The effects of salinity Salinity affects the organism by influencing the density of the medium and through variations in osmotic pressure. I n tropical estuaries the wet season with low salinity is in summer. Though lower salinities may be tolerated at summer temperatures (Moore, 1966) where this drops suddenly and then continues at a low level for a long period stenohaline species are likely to be killed (Nair, 1965a). The reaction of shipworms to different salinities varies widely. Some species can tolerate only high salinities, others can tolerate a fairly wide range of salinities while a few are capable of enduring very low salinities and even fresh water. Further, the salinity tolerance of the same species may vary according t o the geographic location depending on the prevailing temperature and may even vary in the same locality during the different seasons of the year. This is due to the existence of a complex correlation between the biological effects of temperature and salinity, the former having the ability to modify the effects of the latter and change the salinity range of an organism (Kinne, 1963). Loosanoff and Davis (1963) have pointed out that in determining minimum, maximum and optimal salinities, each species, especially those populating estuarine regions, must be studied individually.

THE BIOLOGY OF WOOD-BORING TEREDINID MOLLUSCS

453

The importance of salinity as a limiting factor for the existence and distribution of shipworms has been known as early as 1733. Sellius (1733), Baumhauer (1860) and Harting (1862) noted a correlation between increased activity of shipworms and increase in the salinity of the water. A review of the more important references about shipworms in relation to salinity endurances brings forth the following facts. Bankia setacea, according to Barrows (1917) was very sensitive to a lowering of the salinity in San Francisco Bay. Its lower limit has been determined at 20%, in California (Kofoid, 1921), IS%, at San Francisco Bay (Miller, 1926) and 7-5-13-7%, at the Strait of Georgia (White, 1929). It was also noted (White, 1929) that the species is killed within 1 h at salinities less than 7-5%,, within 6 h at lo%,and within 12 h at 13*7%,. White (1929a) further noticed that this species has two seasonal peaks of breeding corresponding with low temperature and high salinity. During the very low salinities (15-8%,) of winter no breeding was observed. I n British Columbia, Black and Elsey (1948) observed that a salinity range between 9 and 23%, was optimum for B. setacea. The lowest salinity for normal activity of B. gouldi at Beaufort was found to be la%, (Allen and Carter, 1924). Scheltema and Truitt (1954) record B. gouldi in waters with a mean salinity of approximately 9.3%, (range 3.3-15.6%,) at Annapolis, Maryland. According to Nagabhushanam (1961) B. campanellata in Visakhapatnam occurs in areas where the salinity is between 21 and 34%,. The magnitude of the strike decreased with decreasing salinity. Roch (1940) found minimum salinity for normal activity of B. minima to be 32%, and still higher in the Adriatic. B. huwaiiensis lived in fresh water for 2 days and in a mixture of equal parts of normal sea water and fresh water for as long a period as 12 days (Edmondson, 1942). These records give the impression that the genus Bankia is capable of tolerating a fairly wide range of salinities. Teredo navalis (if the determination of the species is correct in all cases) is reported as showing a wide salinity tolerance. M’Gonigle (1926) noted that the boring activity of T . navalis was affected at IS%, and suspended at lo%, in Nova Scotia and a similar result was obtained by Imai et al. (1950) in Onagawa Bay, Japan. Blum (1922) in his classical experiments at San Francisco Bay showed that normal activities were carried on until salinity fell to 9%, but a fall below 6%, was lethal. Individuals living for long periods exposed to low salinities were usually malformed. Miller (1926) noticed that T . navalis in the same locality could tolerate a range of salinity from normal sea water to 9%, and observed that 4%, was lethal in 2 months. Kofoid et al. (1927) fixed the lethal salinity at 5%,. Barrows (1917) found that salinity is an important factor in the distribution of T. diegensis in San Francisco Bay

454

N. BALAKRISHNAN N A I R A N D M. SARASWATHY

and that at least lo%, was required for normal activity. Studies by Edmondson (1942) proved that T . milleri, T . diegensis, T . bartschi and T . trulliformis survived in wood for 12 days in normal sea water diluted with fresh water and that 60 h is about an average period of resistance of various species of Hawaiian shipworms to fresh water. Roch (1940) found the lethal salinity for T . utriculus to be about 28%, and for T . pedicellata 20%, in the Adriatic. On the other end of the scale is the genus Nausitora which is generally confined to brackish water, though some species have occasionally been taken from marine habitats (Nagabhushanam, 1960 ; Nair, 1954). I n N . hedleyi a majority of the adults are typically euryhaline, capable of enduring the whole range of salinities present (0-65-33.68%,) in the environment but with breeding apparently restricted to the low saline period (Saraswathy, 1967). The first record of this genus was by Wright (1864) who obtained specimens of N . hedleyi from fresh water (salinity neither determined nor given), 150 miles above the mouth of the Ganges. Recently Rajagopalaiengar (1964) reported N . lanceolata from Sajnakhali, 24 Parganas District of West Bengal. Hedley (1901) collected N . jluviatilis in the rivers Rewa and Nauva, Fiji and a specimen has been recorded from the Zambezi River in Africa (see Edmondson, 1942). Bartsch (1922) lists four records of Namitora, N . excolpa from the Gulf of California, N . dryas from Peru, N . braziliensis from Brazil and N . fusticula probably from the tropical western Atlantic. From the general locality of Port Jackson, Hedley collected specimens of Nausitora and others were later recorded from Cattai Creek in the Hawkesbury river by Iredale et al. (1932). Watson et al. (1936) reported heavy attacks from a species of Nausitora in the Brisbane river where the salinity is less than lo%, and noticed reduced activity of the shipworm in salinities above 15%,. Populations of N . dunlopei and Teredo poculifer shift up and down the Brisbane River with seasonal changes in salinity. From the same locality Johnson et al. (1936) recorded Nausitora in salinities not higher than lo%, and in the upper George River where the salinity was found ~ .. oahuensis is known from one locality about to be as low as 1 ~ 5 % N Oahu where sea water is diluted by fresh water. N . hedleyi has recently been reported from the low saline waters of Pulicat Lake on the east coast of India (Nair, 1963). These records show that this genus is sensitive to higher salinities and so restricted to estuarine areas. N . hedleyi can apparently withstand wider changes of salinity than allied species like N . dunbpei and is capable of tolerating much lower salinities than typical marine species. Great damage can be expected from species of this genus in the low saline localities of river mouths etc.

Grade KO.

Range ~

-

-

Range 1 1 ~ 1 0 ~ )

.

-

Range I11 (optimum)

.

Range I V (high)

.

~

~

Range V (too high)

.

Satiire of segmentation nil nil nil

-

1 2 3

1.1 1.91 2.21

nil nil few

4 5 6

3.95 4-36 6.55

30 minutes 30 minutes 30 minutes

.

~

30 minutes

7.81 ___~

-~

~~

.

~

nil nil nil ~

~~

8.73 9.22 9.70 10.21 10.44 11.24 11.91 13.60 14.54 15.32 15.73 16.80

30 minutes 30 minutes 30 minutes 30 minutes 30 minutes 30 minutes 30 minutes 30 minutes 30 minutes 30 minutes 30 minutes 30 minutes

mostly normal mostly normal mostly normal mostly normal mostly normal mostly normal mostly normal mostly normal mostly normal mostly normal mostly normal mostly normal

20 21 22 23 24 25 26 27 28 29 30

17.18 19.52 20.30 21.44 22.41 23.42 25.26 ~ 27.14 28.15 30.52 33.84

30 minutes 30 minutes 30 minutes 30 minutes 30 minutes 30 minutes 30 minutes . . _ _ _ nil nil nil nil

a few normal

_

4 hrs

40

a few normal a few normal a few normal mostly abnormal mostly abnormal mostlv abnormal _ ~ ~ _ _ _ _ nil nil nil nil

_.

-

~

8 9 10 11 12 13 14 15 16 17 18 19

~~

nil nil 4 hrs

nil abnormal normal, some abnormal normal some abnormal __

~~

I'cieentnge of ntwing embryos __ .. nil nil nil .~ nil nil 40

Beginning of nzocenaent

~

~

7 ~~~

Extrusion of polar body

-

~~~

.

Range I (too lorn)

Salinity p.p.t.

4 4 4 4 4 4 4 4 4 4 4 4

.5() 6() 65 65 75 80 80 85 82 65 65 50

hrs hrs hrs hrs hrs hrs hrs hrs hrs hrs hrs hrs

few at 4 hrs feu at 4 hrs fe\v a t 4 hrs few at 4 hrs w r y few nil .

nil nil nil nil

1111 1111

1111 ~

__

35 30 2( ) 15 15

~

.

..

~~

iiil nil nil nii

456

N. BALAKRISHNAN NAIR

AND M. SARASWATHY

where species sensitive to low salinities cannot survive. Thus the genus Nausitora effectively occupies an ecological niche and so extends the zone of opcration of shipworms to river mouths and even farther upstream. The construction of dams both for hydroelectric power and irrigation across the rivers and the consequent check on the river flow may lead t o greater spread of tidal water upstream and this can result in the extension of shipworm activity. Psiloteredo healdi is reported as a freshwater form from Miraflores Lake, Panama, Lake Maracaibo, Venezuela and other freshwater lakes and streams on the north coast of South America. References t o salinity tolerance of shipworm larvae are few. Scheltema and Truitt ( 1954) have reviewed previous observations indicating that larvae cannot tolerate the lower limits of salinities which can be endured by adults. M’Gonigle (1926) finds lo%, detrimental t o Teredo navalis larvae. Edmondson (1942) noticed that (‘60 h is about an average period of resistance of various species, of Hawaiian shipworms to fresh water, and that the larvae could survive only for much shorter time.” Observations at Cochin on Nausitora hedleyi suggest (see Table X) that for the early development of the species the most suitable salinity range is from 11.24-14.54%,. Above and below this segmentation was abnormal and the percentage of normal embryos declined. I n salinities lower than 4.36 and above 27.14%, there was no evidence of development (Saraswathy, 1967). Loosanoff and Davis (1963) have observed in the case of oysters that the older the larvae the better they withstood salinity variations. Most species of shipworms require normal marine conditions for successful spawning but the adults may withstand unfavourable conditions by closing the burrow with the pallets. They are also able to utilize stored glycogen under anaerobic conditions.

C. Occurrence in fresh water Shipworms are not limited to the sea and brackish water. Nausitora dunlopei has been reported in timbers in the river Comer, a tributory of the Ganges, 150 miles above the mouth where the water is fresh (Wright, 1864) and in similar situations in Brisbane, Queensland (Johnson and Moore, 1950). Mariot (1965) reports from Cochin China that teredo ” is found in timber structures and in submerged branches of mangroves in the river Saigon which carries almost fresh water. Shipworm activity has been reported in almost fresh water up the Mississippi river (Putnam, 1880), from the Rewe river, Fiji (Steel, 1896), Brazos river, Texas (McGlone, 1914), Upper Pedro Miguel Locks, Panama canal (Embree, 1922), Chulalongkorn Lock in the Rangsit

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canal in Thailand (Bartsch, 1927),Upper Passaic river, New Jersey, in the Sacramento river, California, in the Apalachicola river, north-west Florida and north of New Orleans (Von Schrenk, 1935),and Mira Flores Lake, Panama canal zone (Smith, 1944).

D. Illumination Experiments on settlement of Teredo pedicellata and Bankia Jimbriatula on test surfaces under various conditions of illumination have shown that the attack is greatest at an intensity of 166 foot candles (Isham et al., 1951). These authors also tested the locomotor reactions of the larvae of Teredo pedicellata to various intensities of diffuse and unidirectional light and noted that only the free-swimming larvae are affected by light and not the crawling ones. General conclusions regarding the probable behaviour of larvae under natural conditions were (1) at night the larvae are likely to concentrate at the water surface but tend to remain in deeper water during the day, (2) attachment to timber may be expected to be greatest at an illumination of 160 foot candles which in fact represents deep shade. The latter conclusion has been confirmed by the observations of Owen (1953) at Loch Ryan in Scotland, where horizontally placed timbers were attacked more heavily on the shaded under surface than on the vertical surfaces, obliquely driven piles showing heaviest attack at the sharp angle above the mud line.

E. Settlement in relation to light and gravity The effects of light and gravity upon the intensity of attack by Teredo furcillatus ( = T . furcifera) and Bankia campanellata have been investigated at Visakhapatnam harbour (Nagabhushanam, 1959b). The larvae of Teredo furcillatus settled in any range of light intensity except under conditions approximating to total darkness. In contrast, Bankia campanellata settled most abundantly on the least illuminated panels. The study of settlement of the larvae upon wooden surfaces held at different angles showed that the greatest intensity of settlement occurred on the underside of the horizontal surface and that the intensity of attack decreased as the angle of the surface increased. F. Role of primary jilm Nagabhushanam (1959~)observed that in 30 days, 124 larvae of Martesia striata settled on filmed blocks and 2 on clean ones while in the case of Teredo furcillatus 161 settled on the former as a,gainst 32 on the latter. Moreover a greater number of larvae metamorphosed on the filmed blocks. These experiments suggest that the primary film

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facilitates the rapid settlement. A gregarious tendency has also been reported (Nagabhushanam, 1959a), a distinctly greater number settling on experimental panels previously infested with the adult borers than on the controls. Contrary to the findings of Nagabhushanam (1959a) Karande et al. (1968) noted that the settlement of T .furcifera in Bombay harbour was independent of both light intensity and the presence of a primary film comprised of bacteria, algae or fungi since larvae settled and grew even on sterilized, " clean " timber blocks, the latter being maintained in sterilized sea water for a number of days. According to Karande et al. (1968) it is the softening effect of sea water, rather than the microfilm that helps borer larvae to abrade the wood.

G. Marine fungi and shipworm attack Wood infesting bacteria and fungi, especially in the Ascomycetes and in the Deuteromycetes (Fungi imperfecti), participate in a sort of " conditioning " of the timber, preparing it for the subsequent attack by borers. This is a biological phenomenon, the importance of which has only recently been stressed (Becker and Kohlmeyer, 1958 ; Kohlmeyer, 1963). The activity of these fungi leads t o wood deterioration called " soft-rot ". They are resistant to preservatives and release a strong cellulase which hydrolyses the dignified cell elements leading to the softening and disintegration of the outer tissues of timber. Even though the damage is not spectacular, and may not even be noticed by the layman, their steady activity following submergence prepares timber for attack by crustacean and molluscan borers. These in turn help the fungi to spread from superficial layers to the very core of the timber. Fungal infestation on light timbers of catamarans, dug-out canoes and other fishing crafts, according to Becker and Kohlmeyer (1958), is not of the usual superficial type, the penetration being deep, affecting the entire log. The periodic drying of these logs accelerates the spread of the fungal hyphae which get effective ventilation through the large vessels of these light timbers. Our studies at Cochin harbour have revealed the existence of the following species of marine fungi in the timber test panels. Gnomonia longirostris Cribb and Cribb, Halosphaeria quadricornuata Cribb and Cribb, Torpedospora radiata Meyers, Corollospora pulchella Kohlm., Schmidt and Nair, and Lulworthia sp. (Nair, 1968). The exact role played by these fungi in the ecology of shipworms is under investigation. Recent work on the fungal deterioration of wood in the sea includes taxonomic studies by Cavaliere (1968), Hughs (1968), Johnson (1968), Kirk (1969 b), Kohlmeyer (1968 a, b, c, d), and Tubaki (1968, 1969) and

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ecological studies by Kirk (1969 a), Jones (1968 a, b, c, 1969) and Meyers (1968).

H. The effects of water currents upon the rate of attack of shipworms The rate of water flowing over them is of considerable significance in the distribution of sessile marine invertebrates. Rock-dwelling species may be favoured by the scouring action of strong tidal current which prevents the accumulation of sediment. I n addition to this, the tidal currents carry oxygen as well as food. Gutsell (1930) observed that growth of scallops was most rapid in those positions of the Bogue Sound near Beaufort exposed t o swift tidal currents. Prytherch (1929) found that larvae of Ostrea virginica settled in greatest numbers on the leeward side of submerged objects where the current was least. Hopkins (1937) on the other hand noticed that larvae of the Olympia oyster settled more abundantly on exposure plates that were set parallel with the current than upon those set perpendicular to it. Similar studies, though of great practical interest, have rarely been made on marine borers. Edmondson (1949) found that in Hawaii borers are less prevalent in areas with strong currents than in bays and harbours. Doochin and Smith (1951) determined the limiting velocity for the attachment of Teredo pedicellata to be between 1.4 and 1.8 knots whereas the attack of the isopod, Limnoria, was prevented by currents of between 1.5 and 1.9 knots. The effect of water currents upon the rate of settling of Teredo furcillatus (= T .furcifera) and Bankia campanellata on timber has been studied by Nagabhushanam ( 1 9 6 1 ~ at ) the Naval Base in Visakhapatnam harbour on the east coast of India. He observed that these borers “require some water current velocity for settling on timber and that they settle more rapidly when the waters are flowing than when the waters are still ”. Probably a flow is beneficial in carrying larger numbm of larvae to the test site.

I. Oxygen content of the water Teredo navalis collected from test panels exposed at Kristineberg, Sweden seemed to be little affected by the oxygen content in the water, the animals remaining active even when this fell t o 0.98 mg/l. In the medium, oxygen values of 9-59-10-30 mg/l. were measured (Roch, 1932). This species is known to remain tightly closed in its burrow for long periods with no overt signs of injury (Roch, 1931), when the oxygen content in the burrow must be greatly reduced. Survival is probably due to the high glycogen content with efficient mechanisms for anaerobic glycolysis (Lane, 1959a). During such periods investigators (Lane et al., 1955), noticed decrease in glycogen concentration from 34.0 to

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14.3% in 23 days and a corresponding rise in lactic acid (0.02-0.32%) and pyruvic acid (0.01-0.025%) levels.

J. Hydrogen-ion concentration Allen and Carter (1924) found specimens of Bankia gouldi at Beaufort sensitive to increased acidity (pH 2.3) of the medium and Mawatari (1950) determined the lethal limits for the Japanese species to be about pH 2-3.

K. The effects of turbidity Turbidity is an important factor especially for the inhabitants of shallow coastal waters and of estuarine regions where turbid conditions are often created by heavy rains and consequent river discharge, wind action, dredging operations, boat and ship traffic, etc. I n the tropical regions during the time of the monsoons highly turbid conditions may exist for weeks or even months. Presence of silt affects organisms by providing food (Spooner and Moore, 1940) and influences the transparency of the water affecting the rate of organic production. Denison (1852) recorded that muddiness of the water could destroy shipworms in timber in the harbour at Hobart, Tasmania and at Halifax in Nova Scotia. The apparent immunity from borer attack of the base of the piles of Kidderpore Docks in Calcutta has been attributed to the silty and muddy bottom (Devenish-Meares, 1904). MacKenzie (1927) and Nair (1962) have reported that both crustacean and molluscan borers are much less active where the bottom sediment is being continually churned up by propellers.

L. The effects of pollution The habitats of shipworms, especially those in estuaries, harbours and similar situations, are subject to the effects of pollution either through industrial wastes or by human sewage. The pollutants may consist of solid matter or soluble chemicals of a toxic nature, the presence of which can affect the organisms directly or they may influence the water, for instance its oxygen content (Tully, 1949). However, some effluents appear to be beneficial (Specht, 1950; Hart et al., 1933). Hartley (1840) noted that waters with heavy sewage pollution, or which were influenced by H,S, were comparatively free from shipworms. Similar observations have been recorded from New York harbour by Jarvis (1855), Buren (1875) and Hoag (1905); from San Francisco Bay by Hill (1922) ; and from Marseilles by Henry (1909);

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hvy Salvador and Prudon (1930). Poblete (1916) found that piles driven near the discharge outlet of a gas plant in Valparaiso Bay remained unattacked while Nicholson (1925) and Wedekind (1950) record that oil pollution can keep teredo out of untreated timbers. When the pollution abated attack was resumed. That pollution of harbour waters is unfavourable for shipworm activity is also evident from the studies of Roch (1926) and Nair (1962). Nair (1962) observed that the activity of mat-forming fouling organisms over timber structures in areas with sewage pollution, such as the Bergen harbour, is beneficial since these organisms form a protective cover against the

h a . 48. Four wooden test panels showing the nature of marine fouling organisms chiefly ascidians and polyzoans. (From Nitir, 1962.)

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settlement and penetration of borers. Atwood (1935) points out that sewage in itself has little effect but prolonged high pollution may lead to oxygen depletion which may inhibit the borers but Wedekind (1950) does not subscribe to this view.

M. The effects of marine fouling Lehmann’s (1841) finding at Kyholm in Kattegat that wood covered with colonies of Mytilzcs is apparently immune to attack by ship worms, the dense mat of byssus threads acting as a mechanical barrier against the entrance of their larvae, represents one of the early observations on the effect of marine fouling on borer activity. Tests by Weiss (1948) Redfield and Hutchins (1952) and Nair (1962) have shown (Fig. 48) that dense fouling accumulations over underwater surfaces can effectively inhibit the attack of both crustacean and molluscan borers. The effect of undisturbed fouling on settlement has d s ~ been studied by Johnson et al. (1936), Johnson and McNeill (1941),

FIG.49. A test panel with foulers scraped off to reveal the superficial tunnels of crustacean borers. (From Nair, 1962.)

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Watson et aZ. (1936) and Clapp (1946) who found correlations between fouling and borer infestation, the former inhibiting the settlement of borers by serving either as a mechanical barrier for shipworm larvae or by utilizing them as food. Of the different groups o i fouling organisms, the barnacles are perhaps the most effective agents hindering attachment of shipworm larvae (Anon, 1943; Redgrave, 1920; Von Schrenk, 1935) although other mat-forming organisms (Fig. 50) may also serve tw a protection (Nair, 1962). Nagabhushanam (1960a)found that fouling has a profound effect on the attack of marine borers, fouled blocks ehowing only about one-ninth as much attack as did weekly cleaned panels.

ha. 60. Wooden test panels showing fouling by the polyzoan Cryptosula pallasiana, top; and by tubioolous polychaetes and algae, bottom. (From Nair. 1962.)

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F ra. 51. Typical examples of tropical marine fouling :top, Barnmles (Bdanw,amphitrite conamunis); centre, Mussels (Modiolw, sp.); bottom, Oysters (Crassostrecc sp.).

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FIa. 52. Wooden test panels showing, top, the entranoe holes (white specks) of shipworms ; bottom, the distended siphons. (From Nair, 1882.)

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N. Relation to other borers The mode of attack by molluscan and crustacan borers is very different. To some extent this enables the various borers effectively to share without serious competition the common and limited substrate. The crustaceans work from the outside producing a multitude of minute holes giving the wood a lace-like appearance and a sponge-like texture (Fig. 49), but the molluscs especially the shipworms penetrate deep into the heart wood. Their combined action converts the wood into a highly porous, weak and fragile mass. The crustaceans are also able to enter the creosoted outer surface of treated timber which the shipworm larvae cannot do. Crustacean borers such as Sphaeroma, Limnoria and Chelura may be found in close association with the shipworms on a submerged piece of timber. On the Atlantic coast of Canada an interesting ecological relationship has been reported between hydrographic conditions and the occurrence of borers like Limnoria and Teredo by M’Gonigle (1925). Whereas a higher salinity with lower temperature favours the activity

FIG.53. Underwater photographs showing the distended siphons of shipworms. (From Nair, 1962.)

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of Limnoria, a lower salinity with higher temperature is better for Teredo. The author also noticed that Limnoria can protect piling from Teredo if the latter do not attack too heavily during the first season. A similar view has been expressed by Cormio (1947). That heavy crustacean attack may assist in the destruction of shipworms has also been reported (Walsh, 1920; Miller, 1926; Roch, 1937) although the process involved has not been clearly explained. It is probable that heavy crustacean attack may lay bare the ends of the teredinid tubes exposing them to mechanical damage and even killing the animals.

0. Parasites and associates The role of molluscs as hosts of zoo-parasites has been well known for over two centuries. Much detailed work has been done in recent years regarding the host-parasite relationships. Great interest has been shown in the symbionts of marine molluscs, partly owing to the economic implications and also on account of a general surge of interest in marine biology. Even here, greater attention was naturally paid to

FIG.54. The nature of damage by shipworms. Top, the wooden hull of a boat from Norway; bottom, part of a pile showing the superficial attack by crustacean borers and deep tunnelling by shipworms. (From Nair, 1962.) A.X.H.-9

16

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FIQ.55. The nature of damage by shipworms (continued). Top, test panels sectioned to show the nature of damage by shipworms; bottom, sections of piles to show attaok by Nototeredo norvagioa. (From Nair. 1959).

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economically and potentially important parasites of oysters, clams and mussels (see Cheng, 1967). It is indeed very strange that, despite their great economic importance, no detailed study has been made of the parasites and associates of wood-boring organisms. Several organisms are associated with shipworms in their natural habitat but so far no cause-and-effectrelationship has been established. There is always the possibility that certain parasites and predators may be utilized as effective agents of biological control. Protozoa parasitic in marine molluscs of commercial importance have, however, recently been reviewed by Cheng (1967). All known protozoan parasites of shipworms belong to the ciliata. I n 1887 Durand noticed the occurrence of several protozoan parasites in Teredo navalis but did not name them. Nelson (1923) described a heterotrichous ciliate Boveria teredinidi infesting the gill lamellae of Teredo navalis and Bankia gouldi in Barnegat Bay, New Jersey and observed (Nelson, 1925) that the parasite does no apparent harm to its host. This species has subsequently been reported from San Francisco Bay (Pickard, 1927) also without apparent pathogenic effects. According to Pickard this ciliate does not invade the tissues of its host. Nevertheless, developmental stages of certain parasitic protozoans, probably those of Boveria have been described by Ikeda and Ozaki (1918) in the mantle tissue of Teredo. Levinson (1941) has described a new species B. zenkevitchi from the branchial cavity of T . navalis in the Bay of Sevastopol, the infestation in this instance is reported as taking place as the shipworm penetrates the wood. The holotrich Architophryu sp. has also been reported as parasitic on shipworms (Grave, 1928 ; Roch, 1940). Recent studies by Santhakumari in our laboratory have brought to light an interesting fauna of protozoan associates from shipworms (see Nair, 1968). So far we have collected species belonging to Boveridae, Urceolaridae,Thigmophryidae, Spirostomidae, Licnophoridae, Hysterocinetidae, Stentoridae, and also Zoothamnium, Lagenophrys and Tvochilioides. Detailed taxonomical and ecological studies on these protozoans are in progress. Association between hydroids of the genus Eugymnanthea (Fig. 56) and bivalves has been reported from time to time (Palombi, 1935; Cerruti, 1941; Mattox and Crowell, 1951; Yamada, 1950; Crowell, 1956). The first record of this interesting association between a hydroid recognizable as belonging to Eugymnanthea and shipworms has been by Santhakumari and Nair (1969) who reported its occurrence in Nausitora hedleyi and Teredo furcifera from Cochin backwaters, south-west coast of India. This hydroid, however, differs from all previously describcd

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FIG.56. Eugymnanthea sp. A colony pulled out from the gill of Nausitora hedleyi showing the nature of branching, the basal disc, the polyps and the gonophores.

species of Eugymnanthea in the nature of the polyps which are not solitary but branched. The incidence of the hydroid is seasonal in this locality during the period November to May with nearly 100% infection in shipworms collected during the period December to March, an infestation which is remarkably intense when compared with earlier observations in other bivalves. The number of colonies present in a host ranged from 1 to 80 and the hydroid was found exclusively attached to the ctenidia. Attachment is by a basal disc which is firmly implanted within the tissue of the ctenidium and is further strengthened with the aid of protrusions or " holdfasts " that project from the basal disc-a feature very different from that in species of Eugymnanthea previously studied. There is no evidence of fatal damage to the host tissue. Despite heavy infestation the host specimens are apparently healthy and normal. The more intimate nature of the association and the tendency towards colony formation are interesting features. Recent

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studies of Santhakumari (1970) on the medusa of this form have shown that the species is assignable to the genus Eutima and has, therefore, been named as Eutima commensalis. At Barnegat Bay, New Jersey an interesting case of predator-prey relationship between a ctenophore Mnemiopsis sp. and shipworm larvae was observed during 1921-23 by Nelson (1926a). An inverse correlation was noticed between the abundance of the ctenophore and the intensity of shipworm infestation owing to predation by the ctenophore on the larvae. This shows that the intensity of shipworm attack in a locality could be influenced by the presence or absence of such predators. Two species of turbellarians have been reported associated with shipworms, the first record was by Schmidt (1886) of Grafilla brauni, a rhabdocoele turbellarian parasite living in the digestive diverticula of Teredo at Lesina ( N . E . Adriatic) but has not been reported since its first description (Roch, 1940; Cormio, 1947). Hyman (1944) described a polyclad turbellarian Taenioplana teredini as living in empty teredo burrows in the Hawaiian Islands. She assumes that this turbellarian feeds upon, and may be an important enemy of, the shipworms.

Fro. 57. Some associates of shipworms. Teredicolu typicu Wilson, an internal copepod parasite of shipworms of Hawaii : (a) mature female with egg strings ; (b) mature male (after Wilson) ; (c) general view of a turbellarian Tuenioplunu teredini ; (1) marginal eyes; (2) cerebral eyes; (3) pharynx; (4) sperm ducts; ( 5 ) seminal vesicle; (6) male pore; (7) cement, glands; (8) female pore. (After Hyman, 1944.)

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Edmondson (1942, 1945, 1946b) also reported the incidence of this species at Hawaii especially in the burrows of Teredo milleri. Moll (1939) observed “ cocoons ” of a turbellarian identified as Stylochoplana sp. in inhabited burrows and considers that it is more probably a scavenger. Rancurel (1954b) has reported the occurrence of an acanthocephalan in the ovarian mass and cysts of trematodes infesting the exhalant siphons of Teredo petiti Recluz collected from the west coast of Africa. Of the many natural enemies of shipworms few have attracted greater attention than the polychaetes. These are usually found in close association with submerged timber and more often within the empty burrows of shipworms. There is no agreement about the role these worms play in the ecology of shipworms. Are they carnivores, or just casual associates or scavengers? Two species, Nereilepas fucata and Lycastis senegalensis, more especially the former have been repeatedly mentioned as close associates of shipworms. Authors like Rathke (1799), Vrolik et al. (1860a)) Clavenad (1879), Calderon (1893)) Herpin (1935) believe that the worm is a natural enemy of shipworms and Hedley (1901) even suggested the introduction of the European species of Nereis to check the ravages of shipworms in Australia. Others, however, do not share these views, although agreeing that the polychaetes do, a t times, invade the burrows and devour the shipworms (see Calman, 1919 ; Redgrave, 1920 ; Clapp, 1935a ; Roch, 1940). Another view is that these wormsnever prey on shipworms (McIntosh 1908 ; Cormio, 1947). Potamopyrgus ciliatus (Gould) a small prosobranch gastropod, has been recorded from the Congo estuary living in the burrows inhabited by shipworms (Bequaert and Clench, 1941). The exact nature of this association has not been elucidated. Among the copepod crustaceans, numerous species have been reported as “parasites” or as commensals of molluscs (Monod and Dollfus, 1932). Those of commercially important species of molluscs have been recently reviewed by Cheng (1967). At least 2 species of copepods have so far been reported from shipworms : (1) Teredicola typica Wilson inhabiting the infra-branchial cavity of Teredo and Bankia of Hawaii (Wilson, 1942; Edmondson, 1945, 1946, 1946b). Nearly 75% of Teredo milleri collected from Hawaii has been found infested with the parasite. Growth of infested shipworms appears retarded but otherwise they are little affected; (2) Teredophilus renicola Rancurel occurring in the renal canals of Teredo petiti from the west coast of Africa (Rancurel, 1954). An interesting feature is that only females of this copepod were found within the body of the host. Other crustaceans reported in association with shipworms are an

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FIG.58. Associates of shipworms (continued). C h l u r a terebruns: A and B male, dorsal and lateral views respectively ;C and D female, lateral and ventral views respectively. (From Nair, 1958.)

FIG.59. Associates of shipworms (continued).

Limnoria lignorum : dorsal and ventral

views. (From Nair, 1968.)

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amphipod Talorchestia tricornuata and small unidentified balanid cirriped inhabiting teredo burrows (Moll, 1939). Sellius (1733) while speculating on various remedies for, and preventive measures against, shipworms, suggests, among others, an increase in the number of enemies of teredo especially small fishes. Teredo larvae are susceptible to fungus diseases leading to mass mortalities in cultures (Loosanoff and Davis, 1963). XVIII. OBJECTSATTACKED With their characteristic boring habits and a boundless appetite for wood the shipworms attack vegetable matter of every description both living and dead. The record of their ravages reveals a long list of objects from the sea, brackish waters and also from fresh water. Roonwal (1954) reports from the 24 Parganas forest division in the Sundarbans in West Bengal, that the shipworm Bactronophorus thoracites attacks several species of both living and dead forest trees in the mangrove swamps. The borer attacks trees whose base it riddles with galleries so that ultimately, although the trees remain green and outwardly healthy, they break at the base and topple over in strong wind. Similar destruction has been recorded by Moll (1941a; see also Roch, 1953) from the Philippines. The attack of shipworms is not confined to objects like wooden hulls of boats, barges and docks (Dampier, 1697; Cook, 1773; Moll, 1912, 1948a; Tarasov, 1943; Cormio, 1947; Bavendamm and Schmidt, 1948 ; Nair, 1958 ; Vanin, 1950; Roonwal, 1954) but also to such objects as buoys and floats which they indiscriminately attack. Stimpson (1851) and Clapp (1949) report on the serious damage by Teredo dilatata on pine buoys and slipping at Lynn and Marble Read (N.E. Massachusetts). T . megotara attacks floating pine wood at Newport (Rhode Island) and cedar buoys at New Bedford, and Provincetown (Mass.), and in West Indies (Verrill, 1873), large floats at Norfolk (Durand, 1887) and cedar wood buoys at Woods Hole (Sumner et al., 1913). Shipworm also attacks floating objects like cork (MacGillivray, 1845; Jeffreys, 1859; Marshall, 1893) corky seeds and coconuts (Rpengler, 1779, 1784 ; Martens, 1894 ; Smith, 1910 ; Roch, 1937 ; Crichton, 1941), jute or gutta-percha covers of submarine cables (Jona, 1913; Jungersen, 1906; Rivera, 1915; Roch, 1937, 1940; Cormio, 1947; Bavendamm and Schmidt, 1948), ropes (Coe, 1933a; Clapp, 1934, 1936 ; Roch, 1937, 1940 ; Bavendamm, 1948), plywood (Pessin, 1946) and lobster traps (Rathbun, 1880; Dow, 1950). All fixed objects of plant origin too are unsparingly attacked such as pillars of piers (Nair,

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1959) wharves, stakes, poles, etc., wooden water tanks in ships (Kirkbride, 1922) as well as oyster culture equipment (Nelson, 1922, 1924a ; Roughley, 1925, 1925a; Needler and Needler, 1940; Needler, 1941).

XIX. DETECTION AND PREVENTION OF SHIPWORM ATTACK The protected, entombed life of shipworms has necessitated special and sometimes novel devices to detect their presence. I n their natural habitat they may be found with the help of divers (Clapp, 1936) who can look out for the display of siphons. Since these borers produce a characteristic rasping sound while abrading wood, engineers use electrical stethoscopes and microphones to detect them during inspection of piles (Anon, 1926 ; Tarasov, 1943). X-ray photography has also been employed for the detection and study of shipworms (Ralph and Hurley, 1952). The utilization of stereo-radiography by adding the third dimension was more successful in clearly demarcating the intertwining burrows (Crisp et al., 1953). These methods have facilitated not only detection in timbers but also details regarding the growth rates of the calcium-lined burrows without damaging the substrate and disturbing the animals. I n Ohio, gamma rays (Cobalt 60 and Iridium 192) have been used for the radiographic inspection of underwater sections of piles (Jelley, 1953). Since the beginning of man's maritime activity, he has been trying every known mechanical, chemical, electrical and biological means t o deter, discourage or destroy these pests. As early as 1697, Dampier, in his account of his voyages round the world, describes a method, believed by the natives of Mindanao in the southern Philippines to be effective in checking their attacks. Drydocking the vessel soon after each voyage, they char the vessel's outer bottom with a view to drying it completely. This they claim to be a preventive measure. An identical method has been practised by the fishermen of Bengal who suspend the boat infested by shipworms across two poles and light a fire beneath to destroy them. The charring of the bottom hinders further attack for a period (Wright, 1864). This method is based on the fact that desiccation is fatal for these soft bodied creatures and is practised with suitable modifications in various countries. I n Sydney timbers have thus been treated with the " Carbo-Teredo " process (Anon, 1916, 1917) which consists of impregnating the timber with a hydrocarbon and then charring the outer surface by means of a heater rather than by open fire (Cunningham, 1920, 1923). This method has been found effective for certain types of timber (Hamer, 1920, 1923, 1924, 1925; Holderness, 1931). Since desiccation is fatal to shipworms this end could

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also be achieved by merely hauling the boats out of the water and exposing it to the hot rays of the sun and this very simple and effective remedy has been recommended (Zernov, 1909 ; Orton, 1914 ; Grave, 1928 ; Erlanson, 1936). Since exposure to fresh water is lethal for typical marine species, mooring the vessels in regions of low salinity has also been recommended (Weiss, 1917 ; Baughman, 1949 ; Nair, 1965). Unfortunately during such operations, the borer can seal itself within its burrow and remain alive for long periods of time. Therefore, the exposure to this unfavourable medium must be sufficiently long to kill the borers. Other protective methods include introduction of poisons into the surrounding water to create a toxic environment in the immediate vicinity (Walker, 1924; Walker et al., 1926; Johnson, 1948); scupper nailing (Jones, 1910; Von Schrenk, 1927; MacLean, 1941,1954; Edmondson, 1953) ;fixing shingles or glass particles over exposed wooden surfaces (Anon, 1943) or completely sheathing them with boards (Andrews and Graham, 1906; Atwood et al., 1924; Ohsima, 1940; Carr, 1953) metal, concrete or any such suitable wrappings (Dudley, 1905 ;Roessler, 1906 ;Hardesty, 1908 ;Kennon, 1908 ;Davis, 1910 ;Anon, 1943b), metal bands or pipe casings (Stempel, 1903; Kennon, 1904; Smout, 1905; Hunt, 1906; Apfel and Earnest, 1908; Atwood et al., 1924; Upton, 1940; Adams, 1941 ; Johnson and McNeill, 1941 ; Edmondson, 1953) or fixed or floating collars for piles (Walker et al., 1926; Johnson et al., 1936 ; Johnson and McNeill, 1941 ; Johnson, 1948 ; Boas, 1947 ; Chellis, 1948; Allan, 1950; Anon, 1951). The discovery that a severe shocksuch as a blow from a pile driver is detrimental to shipworms within a pile soon found application. Thus dynamite was employed in the vicinity of infested timbers (Neiley et al., 1927 ; Anon, 1944 ; Shackleton, 1949). It has been claimed that a blasting schedule of 2 month intervals increased the service life of piling up to 3-4 years (Dynes, 1945). The procedure consists of detonating from 10 to 12 charges of explosive simultaneously in the water between pilings at low tide. Tests indicate that 75% of teredo infestation is destroyed by this procedure. This effective method is at present extensively used in the Canadian logging industry (Yonge, 1951). Electrolytic protection is yet another device (Clapp, 1926). Here alternating rows of iron and copper nails or strands of copper and iron wire are attached around a pile or wooden surface that needs protection. The electrolytic action taking place in the wood soaked with sea water results in the deposition of iron oxide in the surface layers of the wood and this apparently prevents the entrance of borers. Electrolysis of sea water and the liberation of chlorine etc., as a measure to

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47 7

suffocate and poison the shipworms within their burrows, though suggested repeatedly with interesting modifications (Hooper, 1909 ; Tatro and Delius, 1910; Anon, 1912; Edwards, 1912; Hesse, 1914; Marshall, 1914) was subsequently found to have no appreciable effect on established borers in piles (McQuaid, 1924 ;Fries, 1925 ; Walker et al., 1926 ; Mal’m, 1938). Electrocution as a possible measure to destroy the shipworm, has been tried by passing a current of high amperage and voltage with special devices (Shuffleton, 1901 ; Prudden, 1907). Using appropriate electrodes copper was deposited on the pile for added protection (Howe, 1908). The real effects of all these tests have not been reported. Contrary to the claim for electrocution, Nicholson (1920) got negative results from Table Bay harbour, his wired pieces proved to be more severely attacked than the control pieces! Of the various methods used to protect timber against borer attack, chemical treatments appear to be the most practicable and widely used. From ancient times wood preservation has been practised using different empirical formulae with varying degrees of success. The Egyptians with their expert knowledge in the preservation of dead bodies also developed effective methods for wood preservation. The submarine survey in the Mediterranean by the French Navy brought to light hulls of ancient sailing ships which had remained submerged for more than 20 centuries with timber still perfectly intact. Arabs and Indians also maintained large fleets of sailing vessels both for colonization and commerce. Unfortunately we have no records of the ways by which they preserved timber. The best preservative known is impregnation of timber with creosote (Teesdale and Shackell, 1917 ; Hill, 1922 ; Atwood et al., 1924; Miller and Hill, 1927 ; Ramage and Burd, 1927; Clapp, 1949, Becker and Schulze, 1950) with suitable additives (Emery, 1935 ; Bryan, 1947 ; Mayfield, 1952 ; Richards, 1953; MacLean, 1954). But even this leaches out in time leaving the surface exposed to borer attack. This aspect of the problem is the more acute in warm tropical waters. Recent marine borer studies at the British Columbia Research Council, Vancouver, Canada include among others monitoring studies for marine borer attack (Walden, et al., 1967), sonic testing of marine piling (Walden and Trussel, 1965) and development and possible commercial application of underwater coatings for wood; marine borer protection systems for commercial logs, dry-docks, marine installations and evaluation of the resistance to continuous leaching of modified creosotes, organo-lead compounds and formulations of zinc and chromium compounds. The rate of ingress of borer activity into harbours as a result of the abatement of pollution is also under investigation.

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Perhaps the most economical and effective method for checking ravages of shipworms may be the least tried, namely biological control. Several predators, parasites and associates of unknown relationship are known from shipworms (vide supra)such as protozoans, planarians and polychaetes. Some of these are known to attack and devour them piecemeal. Despite man’s ceaseless fight against shipworms, with all available resources and techniques, their relentless destruction continues and a thorough re-orientation in our techniques of warfare has become imperative. The discovery of an effective panacea depends on a better understanding of the ecology of these specialized bivalves.

XX. TIMBERSOF UNUSUAL DITRABILITY AGAINST SHIPWORMS No woods have been shown to be indefinitely immune to the destructive activity of shipworms. However, certain timbers are known t o possess a greater degree of resistance than others, a few tropical species being accredited with exceptional durability. The exact nature of the repellent properties which protect them against borer attack is not clearly known although the presence of various natural substances in timbers has been shown to inhibit the activity of borers serving either as deterrent agents or as mechanical obstruction. I n the search for a wood that may resist the attack of shipworms, man has tried every type of timber. The details of these elaborate tests are recorded in the annals of harbour engineers from all over the world. These show that some species of timbers exhibit unusual resistance to boring animals, this factor being linked to certain specific properties of the timber. This may purely be on account of the structure or hardness of timbers (Kooy, 1922; Rivera, 1922; Johnson, 1932; Moll, 1948a) or owing to the presence in them of certain deterrent substances (Theophrastus, 1495-98 ; Montanus, 1671) and more specifically resinous materials (Sellius, 1733; Cram, 1873; De Coque, 1895; Hoech, 1896; Valder, 1904 ;Rivera, 1922 ;FitzsimonsandBrooks, 1920;Baldwin, 1938; Moll, 1948), alkaloids (Iterson, 1934; Fitzsimons andBrooks, $920; Barger, 1922,1924 ; Kooy, 1922 ;Record and Mell, 1924 ;Bianchi, 1933 ; Iterson, 1934; Baldwin, 1938; Spoon and Loosjes, 1946; Bavendamm, 1948; Bavendamm and Schmidt, 1948 ; Moll, 1948a, Edmondson, 1955), poisonous inclusions (Bavendamm, 1948), tannins (Moll, 1948 ; Edmondson, 1955), gummy deposits (Anon, 1862 ; Edmondson, 1947), waxy materials or oily substances (Fitzsimons and Brooks, 1920 ; Money, 1811; Jarvis, 1904) ineither thebark orthe body of timber have been cited as responsible for the general durability of certain timbers

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exposed in sea water. Borer resistance has thus been linked with certain inherent physical or chemical properties of timbers. As early as 1495 Theophrastus stated that olive escapes the attack of Teredo because of its bitter taste. The bitter components present in the wood has been cited as an effective repellent against the marine borers and the application of these bitter extracts to non-resistant wood was suggested even in early literature (Anon, 1666 ; Montanus, 1671). Sellius in his monograph has mentioned timbers that are particularly deeply coloured, bitter and resinous which appear to be immune to Teredo attack. The apparent indemnity from shipworm destruction of the famous Jarrah (Eucalyptus marginata) of Australia has generally been attributed to its large content of resinous materials (Anon, 1862). This deterrent substance, however, is not present in decayed Jarrah timber (Du Cane, 1864). Oleoresins, chiefly between bark and sapwood, are present in turpentine, Xyncarpia laurifolia (Fitzsimonsand Brooks, 1920), and resinous tylosus in the famous Greenheart, Nectandra rodioei (Baldwin, 1938). Resinous substances have also been reported from such timbers as Yellow pine (Cram, 1873), and Teak (Rivera, 1922). The Demerara Greenheart (Nectandra rodioei) of British Guiana has long been well known for its great resistance, though not for absolute immunity, to shipworm attack. This resistance is ascribed to the presence of poisonous alkaloids particularly the alcohol soluble bebeerine or nectandrine in considerable quantities (Barger, 1922, 1924 ; Kooy, 1922; Record and Mell, 1924; Bianchi, 1933; Iterson, 1934; Baldwin, 1938; Spoon and Loosjes, 1946; Moll, 1948a). This timber is widely used in Europe and is highly resistant to borers in the harbours of Holland (Thoorn, 1887 ; Kooy, 1922), at Lowestoft, England (Barger, 1924), Liverpool and the piers in the Tyne, England (Baldwin, 1938). Light attack has occurred only after the protective poisonous properties of this alkaloid have been leached out owing to long immersion in salt water (Loppens, 1905; Reyne, 1922; Anon, 1937, 1942). The superficial layer, which alone is attacked, has been shown to contain only 1.6% of alkaloid while the deeper wood contained 5.2% (Anon, 1942). While this timber resists shipworm attack in the cold European waters, its protective qualities are not very effective in the warm tropical waters, probably due to accelerated leaching of the poison. Teredo reyne attacks this timber in the brackish waters of Saramacca Canal in Dutch Guiana (Reyne, 1922; Record and Mell, 1924). Reports from Panama and Guyana (Anon, 1937), also indicate that it is unable to resist attack by Bankia xetaki and Teredo mirajlora in these waters. That accelerated leaching is probably the reason is substantiated by the fact that even

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in the cold waters of Holland and at Nieuport, Belgium (Anon, 1937 ; Loppens, 1905) this timber has been attacked by Teredo when the alkaloid was leached out, the outer alkaloid-free layer alone becoming vulnerable to attack. The presence of alkaloids andother as yet undetermined poisonous inclusions in the tissues is believed to be responsible for the unusual durability and natural resistance of many other timbers such as Iron wood, Eusideroxylon xwageri and Bitter Angelims, Andira vermifuga. Syncarpia laurifolia grown in Australia and in Hawaii lacks resistant properties that give durability in sea water, borers attacking both sapwood and heartwood. Edmondson (1947) regards the presence of gum deposits as a specific factor in the comparatively high resistance of Australian and Hawaiian timbers to marine borer attack. Resistance shown by even the same species of timber is relative depending on such factors as lack of age, rapidity of growth, place of origin, etc. The resistance shown by Huon Pine, Dacrydiurn franklinii (Fitzsimons and Brooks, 1920) and teak, Tectona grandis (Money, 1811) is due to the presence of obnoxious oils. The Naval Research Laboratory of the U.S. Navy has been examining in the past years, the natural resistance of tropical woods to marine borer attack (see Trussel and Jones, 1970). 114 different woods were tested for a 14 month exposure. It was found that no timber available in abundance and of sufficiently large size was found to show resistance to all marine borer species. Dalbergia retusa (cocobolo)was highly resistant in all environments but its potential as a commercial timber is limited. Cordia aliodora, Chrysophyllurn cainito and Bouteria campechiana also showed evidence of resistance to marine borers over the period tested. A few hard heavy woods such as Tabebuia guayacan, Swartxiawe panamensis and Manilkara dariensis are apparently capable of resisting tropical fungi. (See Trussel and Jones loc. cit.). The brackish water shipworm Teredo healdi was found to be more destructive than typical marine forms capable of boring into and destroying even well known borer resistant timbers such as ekki, greenheart and acapu.* A. The role of silica The significance of the presence of silica in the tissues of timber by imparting durability to woods in underwater constructions, etc. has been repeatedly stressed (Iterson, 1934 ; Gonggrijp, 1924, 1924a, 1932 ; Record and Mell, 1924 ; Bianchi, 1932, 1933, 1934 ; Anon, 1938 ; Prison, 1942 ; Spoon and Loosjes, 1946 ; Amos and Dadswell, 1948 ; Amos and Tack, 1952; Horn, 1948). Nanji and Shaw (1925) have shown that nearly 90% of the total silica in plants is present as free silicic acid, *See note added in proof, p. 509.

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probably in a colloidal state whereas the other 10% is probably in combination with a polysaccharide constituent of the plant in a form only t o be extracted after treatment with acid. According to Gonggrijp (1932) the capacity of woods to repel marine borers seems to be correlated with the high silica content together with the compactness of the tissue. Timbers possessing exceptional powers of resistance to marine boring organisms have been reported from the Pacific Islands, Indonesia, Australia, Caribbean and South America. A majority of the 700 species examined by Prison (1942) from Belgian Congo contained more than 0.50% of silica which is considered as the minimum amount effective against boring animals. Reports by Amos and Dadswell (1948) and the Institute of Paper Chemistry (1951) give an idea of the amount of silica present in timbers. The available data strongly suggest that silica, if present in sufficient quantity, may be an important factor in protection against shipworms.

B. Bark of trees That the intact bark on piling is an effective temporary chemical barrier against shipworm attack has long been known (Jarvis, 1855; Jarvis, 1948; Mobius, 1875; Buchanan, 1877). This is owing to the presence of appreciable amounts of silica, alkaloids, tannins or other substances which offer considerable resistance t o shipworms. The underlying wood, especially the deep inner layers, is devoid of effective concentrations of these defensive chemical components and is, therefore, highly susceptible t o attack. Thus the turpentine timber used in Australian waters (Johnson, 1932; Johnson et al., 1936; Rust and Ferguson, 1935; Jarvis, 1948), the American hemlock (Bate and Westwood, 1863-68), Beech trunk in the Bay of Aabenraa, Denmark (Mobius, 1875), Prickly tea tree in N.S. Wales (Roughley, 1925), Oak piles at Portland, Maine (Jaeger, 1936), Swamp Mahogany in Australia (Boas, 1947) and Sen timber in Yokohama, Japan (Mawatari and Kobayashi, 1952) are all known to offer greater resistance to the ravages of shipworms with the bark intact than without it. Many authors have noted that shipworms will not penetrate wood through the barrier of the bark (Holbrook, 1902; Cameron, 1909; Hamer, 1920; Foxworthy, 1921 ; Ilsley, 1921; M’Gonigle, 1925; Neily et al., 1927; Kramp, 1937; Edmondson, 1955 ; Nair, 1956a). The principle behind using green piles is t o retain the bark without damage and allow it t o adhere to the wood as firmly as pospible during the piling operations (Walsh, 1920), since the value of the bark depends not only on its character and composition but also upon its close adherence t o the sapwood. Experts have, therefore, recommended all possible ways and means for retaining

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N. B S A K R I S H N A N NAIR AND M. SARASWATHY

bark intact without any defective limb spaces and have advised that piles should not be cut or bored through when constructing the wharf and that brazings, etc. should be secured with clamps rather than boreholes for bolts, etc., especially in the intertidal zone (Methven, 1914). The degree of protection offered by barks of timbers in underwater wooden structures varies greatly, not only in different timbers correlated with their chemical characteristics as suggested by Record and Hess (1943), but also from place to place depending on the species of borer involved. In the United States the additional life for bark protected piles has been reported as just a year or two (Hunt and Hill, 1921) while in Australian waters this period is considerably more (Iredale et d.,1932; Rust and Ferguson, 1935). XXI.

ACKNOWLEDGEMENTS

We are deeply indebted to Sir Maurice Yonge, for scrutinizing the manuscript, and for making helpful comments and criticisms. We are grateful to the following for allowing us to reproduce certain figures in this review : Publications Office, Museum of Comparative Zoology, Harvard University, Cambridge, Massachusetts for Fig. 12h from “ A Survey and Illustrated Catalogue of the Teredinidae ” by Ruth D. Turner ; Professor Hans Brattstrbm for Figs. 1, 8, 55, 58, and 59 from the senior author’s article in Publ. Biol. Stasjon. Espegrend, 25, Univ. Bergen Arbok 1959, Naturv. rekke, Nr. 1;and for Figs. 48, 49, 50, 52, 53 and 54 from the senior author’s article in Sarsia, 8, 1962. One of us (M.S.) is grateful to the University of Kerala for the award of a research fellowship during the tenure of which the work on Nausitora hedleyi, Teredo furcifera and Teredora princesae was carried out and to Dr. N. K. Panikkar, Director, National Institute of Oceanography for permission to be associated with this work. XXII.

REFERENCES

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TEE BIOLOGY OB WOOD-BORING TEREDINID MOUWSUS

609

Yonge, C. M. (1926a). Structure and physiology of the organs of feeding and digestion in Ostrea eddis. J. mar. bwl. Ass. U.K.,N.S. 14, 296-386. Yonge, C. M. (1926b). Protandry in Teredo norvqica. Q . Jl microsc. Sci. 70, 391-394. Yonge, C. M. (1927). Formation of calcareoustubes round the siphons of Teredo. Nature, Lond. 119 (2983), 11-12. Yonge, C . M. (1948). Formation of siphons in Lamellibranchia. Nature, Lmd. 161 (4084), 198-199. Yonge, C. M. (1949). On the structure and adaptation of the Tellinacea deposit feeding Eulamellibranchia. Phil. Tram. R . SOC. B. 234, 29-76. Yonge, C. M. (1961). Marine boring organisms. Research (London),4 (a), 162167. Yonge, C. M. (1963). The monomyanan condition in the Lamellibranchia. T r m . R. SOC. Edinb. 62 (2), 443-478. Yonge, C. M. (1957). Mantle fusion in the Lamellibranchia. Pulil. Sta;z. zool. Napoli, 29, 151-171. Yonge, C. M. (1963). Rock-boring organisms. I n “ Mechanisms of Hard Tissue Destruction ”,pp. 1-24. Publ. No. 76, American Associationfor the Advancement of Science, Washington, D.C. Zernov, S. A. (1909). Grundzuge der Vertreitung der Tierwelt des Schwarzen Meeres bei Sebastopol. I. Benthos. Imt. Revue ges. Hydrobwl. Hydrogr. 2 (1-2), 99-123. Zobell, C. E. (1946). “ Marine Microbiology.” Waltham, Massachusetts. Zvorykin, N. P. (1941). Povrezhdeniia i Vosstanovlenie portovykh gidrotekhnicheskikh Soomhenii, 271 pp. Moskva and Leningrad.

Note added in proof.

Bavendamm and Roch (1970) recently investigated the natural resistance of tropical woods against marine borers at Mar Piccolo of Taranto (South Italy) under optimum conditions regarding temperature and salt content of water. The results indicate that the heartwood of E d e r o x y l o n zwageri (Billian or Borneo-Ironwood), of Synmqvia; prooera (Turpentine) and of Owtea rodiaei (Demerara-Greenheart)remained unattacked; that of Lophira procera (Bongossi), Dicorynia paraemis (Basralocus)and Eucalyptus margiirzata (Jarrah) showed very good or moderate resistance. The heartwood of Afrmosicc elata (Afrormosia)of Cyliwdiscus gahnensis (Okan)and of Sarcocephulus diderrichii (Bilingaor Opepe) was not resistant contaxy to other experimental results. According to these authors partly known and partly unknown toxic substances have much greater signifioance than silicious inclusions.

This Page Intentionally Left Blank

Author Index Numbera in italios refer to papa on which the f d l refereme b given

A Abbott, D. P., 15, 16, 30,33,34,47,63, 82, 83, 275, 276, 326, 327 Abbott, W., 209,219,222,224,227,241 Ackermann, D., 206,207,208,209,210, 212, 226, 227, 241, 242 Adams, J. A., 140,192 Adams, L. L., 476, 482 Adanson, M., 345, 482 Ahlstrom, E. H., 273, 274, 309, 315, 324, 326 Albee, R., 275,276,326 Aldrich, F. A., 40, 83 Allan, J., 476, 482 Allan, M. S., 476, 477, 484, 508 Allen, F. E., 79, 83 Allen, I. V. F., 477, 507 Allen, J. A., 7, 40, 83, 219, 240, 242 Allen, K., 205, 206, 207, 208, 209, 210, 212, 213, 219, 221, 222, 231, 232, 239, 242, 251 Allen, M. B., 103,193 Allen, M. S., 453, 460, 482 Alverson, D. L., 273, 315, 324, 326 Amos, G. L.,480, 481, 483 An, H. V., 205, 242 Anderson, G. C., 166, 195 Andrews, G. W., 476, 483 Angot, M., 295, 298, 326 Ankel, W. E., 49, 83 Anonymous, 448, 451, 463, 475, 476, 477, 479, 480, 483 Anraku, M., 129, 159,193 Ansell, A. D., 366, 367, 386, 483, 484, 500 Anslow, G. A., 20, 46, 87 Antia, N. J., 113, 128, 193, 267, 326 A.O.A.C., 433, 484 Apfel, P. F., 476, 484 Apollonio, S., 183, 193 Aqvist, S., 222, 243 Araki, G., 436, 437,438, 490

Armstrong, F. A. J., 105, 156, 193, 325, 326

&back-Christie-Linde, A., 39, 61, 63, 66, 83

ArrheniuEi,G., 262, 326 Arthur, R. S., 260, 326 Ashton, P. A., 152,198 Atkina, D., 376, 484 Atwood, W. G., 462, 476, 477, 484 Austin, J., 1437 151v 201 Austin, K. H., 105, 128,203 Awapara, J., 205, 206, 207, 208, 209, 1489

1529

210, 211, 212, 213, 215, 217, 218, 219, 220, 221, 222, 224, 227, 230, 231, 232, 239, 241, 242, 249, 250, 251

B Bdey I*v.9345, 355y 484 Baker, C. M. A., 152, 198 Bakum, A., 279, 289, 294, 332 Bd, D. V., 341,346,355,365,368,434, 3659

3689

435, 439, 484, 488, 501, 502

Balasubramanian, K., 396, 406, 407, 444, 458, 494

Baldwin, C. E., 478, 479, 484 Baldwin, E., 206, 209, 215, 242 Ballister, A., 293, 329 Bancroft, F. W., 31, 32, 33, 48, 83 BangyN*,2699 286, 326 Basks, R. E., 258, 331 B w e , K., 290, 326 Bm€Pry 40994789 484 Barnes, H., 146, 156, 193 Barrington, E. J. W., 42, 62, 83 Barrows, Barth, L. A. G.,L., 29,453, 83 484 4799

Barth, L. J., 29, 83 Bartach, P., 354, 359, 360, 424, 426, 443, 452, 454, 457, 484

Bascheri, M.C., 205, 238, 242 Bate, C. S., 481, 485 611

612

AUTHOR INDEX

Baughman, J. L., 476, 485 Ba&uer, E.H., 447,463, 485 Bavendamm, W.,474, 478, 485 BaylitT, W.H.,277, 326 Baylor, E.R.,130,193 Beall, D., 460, 491 Bear, R. S.,228, 242 Beaven, G. F.,48, 83 Becker, G.,337,341,342,396,401,409, 410, 413, 443, 458, 477, 485 Bedfmd, J. J., 207, 239, 242 Beers, J. R.,113, 129, 140, 141, 143, 144, 148, 161, 166, 162, 180, 181, 193,197,304, 326 Beeson, C. F. C., 410, 485 Beklemishev, C. W.,136,138,139,140, 170,193 Beklemishev, K. V.,311, 326 Bell, L. G. E., 21, 83 Bellan, G., 42, 83 Bennet, J., 397, 485 Bennett, I.,33, 86 Benson, B. B., 103,193 Bequaert, J. C., 472,485 Bergere, A. M., 206, 212,248 Bergeret, B., 217, 218, 242, 243, 244, 246 Bergeret, R., 218,243 Berner, A., 134, 164, 193 Berner, E.,206, 243 Berner, L.,46, 79, 80, 81, 83 Berrill, N.J., 8, 13, 15, 16, 18, 19, 20, 21, 22, 23, 29, 30, 33, 83, 84 Berrit, G.R.,278, 279, 286, 288, 287, 291, 327 Beuk, S., 367, 485 Beverton, R. J. H., 326, 327 Bianchi, A. T. J., 478, 479,480,485 Bielig, H.J., 3, 84 Bird, H.R.,223, 249 Bishop, Y.M.N.,276, 277, 278, 332 Bjerknes, J., 278, 286, 327 Black, E. C., 397, 416, 419, 463, 485, 486 Blackburn, M., 295, 302,327 Blaschko, H.,215, 217, 218, 219, 243 Blum, H.F., 401, 419, 426, 430, 461, 463, 486, 495 Blunt, C. E.,273, 327 B o d , P.A., 364, 366,486

Boas, I. H., 476, 481, 486 Bogdanov, D. V.,294, 327 Bolin, R.L.,276,276,327 Bonnevie, 72, 84 Boolootian, R.A., 397,490 Boquet, P.L.,206, 243 Borisjak, A.,404, 486 Bostrom, H.,222, 243 Botticelli, C. R.,14, 89 Bouchard-Madrelie,C., 14, 84 Bouchet, J.-M., 40, 84 Bourdillon, A., 54, 84 Bourne, 76, 84 Bouvien, P.,67,84 Bowley, C., 291, 327 Boynton, L.C., 434, 441,486,498 Bradley, H.C.,207, 249 Brandt, C. L.,13, 91 Brandt, K.,143,193 Bresciani, J., 51, 62, 84 Brewin, B. I., 7, 12, 14, 16, 18, 19, 34 32, 33, 63, 67, 68, 84, 85 Bricteax-GrBgoire, S., 207, 208, 208, 210, 212, 226, 233, 236, 236, 243, 247 Broenkow, W. W., 111, 193 Brooks, E.R.,129, 163, 164, 166, 171, 200 Brooks, F. T., 478, 479,480,489 Brown, A. A.,430, 451, 486 Brown, T., 429,451,486 Bruce, J. Q.,279, 288, 289, 333 Bruun, A. F.,69, 85 Bryan, G.W., 82, 85 Bryan, J., 477, 486 Buchanan, J., 481, 486 Budocks Technical Digest, 417, 486 Bulatov, G. A., 396, 486 Bumpus, D.F.,129,139,202,326,332 Burchall, J., 298, 327 Burd, A., 317, 334 Burd, J. S.,477, 503 Buren, J. D.Van, 460, 486 Bursa, A. S., 184, 185,193 Burton, J.D., 163,193 Butler, E. I., 137, 140, 141, 143, 144, 147, 151, 162, 164, 166, 166, 167, 168, 169, 162, 167, 169, 170, 193 BUYS,M.E. L., 279, 286, 327

AUTHOR INDEX

C Cabioch, L., 42, 85 Calder, D. R., 43, 85 Calderon, S., 472, 486 California, Department of Fish and Game, 266, 272, 273, 278, 304, 327

Calman, W. T., 472, 486 Calvin, J., 61, 96 Cameron, J. B., 481, 486 Camien, M. N., 212, 233, 243 Caperon, J., 123, 194 Carlisle, D. B., 4, 21, 29, 35, 36, 81, 85 Carlson, B., 212, 245 Carpenter, E. J., 124, 194 Caspine, C., 45, 85 Cam, D. R., 476, 486 Carriker, M. R., 405, 486 Carruthers, J. W., 290, 327 Carter, R. H., 453, 460, 476, 477, 482, 508

Cwsie, R. M., 8, 86 Castagna, M., 32, 97 Castle, W. E., 13, 86 Caullery, M., 30, 86 Cavaliere, A. R., 458, 486 CavaJlini, D., 215, 219, 220, 222, 243, 244

Cergignon, F., 293, 329 Cerruti, A., 469, 486 Chanley, P. E., 404, 496 Chapeville, F., 215, 244 Chari, S. T., 434, 507 Chetagner, F., 217, 218, 242, 243, 244, 246

Chau, Y.K., 131,194 Chellis, R. D., 476, 486 Cheney, S., 448, 451, 487 Cheng, T. C., 47, 86, 469, 472, 487 Christensen, H. N., 233, 244

Chu, S. P., 104, 121, 194 Ciereszko, L. S., 206, 227, 244 Clancey, E. J., 459, 495 Clapp, W. F., 364, 366, 399, 401, 419, 426, 448, 463, 472, 474, 476, 477, 484, 487, 504 Clark, F. N., 309, 327 Clark, H. L., 59, 86 C l a v e d , A,, 472, 487

613

Clench, W. J., 472, 485 Cloney, R. A., 20, 21, 86 Clutter, R. I., 302, 328 Coatsworth, J. L., 114, 117, 196 Coe, W. R., 345, 390, 391, 394, 396, 399, 406,474, 487

CoEn, C. C., 270, 329 Cogate, S. S., 290, 327 Cole, H. A., 50, 81, 86 Cole, L. J., 474, 506 Comita, G. W., 165,195 Conklin, E. G., 13, 86 Conover, R. J., 135, 136, 137, 130, 140, 141, 148, 149, 151, 153, 156, 161, 165, 169, 170,194 Conover, S. A. M., 107, 108, 126, 187, 188, 189,194, 202 Cook, J., 474, 487 Cooper, L. H. N., 106, 115, 129, 132, 136, 137, 139, 143, 152, 154, 194, 197, 270, 329 Copenhagen, W. J., 279, 327 Corcoran, E. F., 295, 296, 328 Cormio, R., 467, 471, 472, 474, 48 7 Corner, E. D. S., 129, 131, 134, 135, 136, 137, 139, 140, 141, 142, 143, 144, 145, 146, 147, 148, 149, 151, 152, 154, 155, 156, 157, 158, 159, 162, 163, 164, 165, 166, 167, 169, 170,193,194,195,198,209,2 '44 Corwin, N., 107, 108, 128, 173, 174, 175, 176,198 Costa, S., 4, 36, 40, 41, 86 Costello, D. P., 402, 487 Coward, 5. J., 131,197 Cowey, C. B., 129, 131, 134, 136, 139, 142, 145, 146, 147, 148, 149, 151, 152, 154, 155, 159, 162, 163, 164, 165, 166, 167, 169, 194, 195, 209, 244 Craig, H., 103, 195 Cram, T. J., 478, 479, 488 Crichton, M. D., 474, 488 Crisp, D. J., 425, 475, 488 Crokaert, R., 226, 251 Cromwell, T., 261, 292, 328 Crowell, S., 469, 488, 497 Crozier, W. J., 60, 86 Cunningham, J. E., 475, 488

514

AUTHOR INDEX

Curl, H., 293, 328 Curl, H., Jr., 140, 141, 145, 195 b i e , R. I., 258, 259, 260, 279, 286,

Donadio, G., 238, 244 Dons, C., 363, 364, 415, 426, 446, 447, 448, 450, 488

Doochin, H., 459, 488 Dore, W. H., 401, 419, 425, 430, 434,

329

Curtis, D. R., 239, 244 h h i n g , D. H., 264,265,267,270,307,

441, 443, 451, 453, 488, 495

310, 318, 328

DOW,B., 474, 488 Dragovich, A., 34, 81, 86 Dresel, E. I. B., 152, 195 Drisko, R. W., 208, 210, 244 Droop, M. R., 64, 86, 123,195 Du Cane, E. F., 479, 488 Duchhteau, B. G., 210, 237, 246 Duchhteau, G., 207,208,210,212,

D Dadswell, H. E., 480, 481, 483 Dakin, W. J., 33, 86, 130, 199 Dalpont, G., 115, 196 Dampier, W., 474, 475, 488 Danielsson, H., 228, 249 Darbyshire, M., 258, 264, 279, 286,

233, 234, 235, 236, 243, 245 Dudel, J., 210, 239, 246 Dudley, L. E., 476, 489 289, 328 Dudley, P. L., 60, 90 Das, S. M., 63, 86 ‘ Duerr; F. G., 207, 233, 250 Datta. S. P., 218.,~ 219. 243 Dugdale, R. C., 103, 116, 119, 120, 121, Davidson, M. E., 402, 487 182, 195,196, 198 Davies, A. G., 123, 195 Dupr6, S., 220, 244, 245 Davies, D. H., 309, 315, 328 Durand, W. F., 474, 489 Davis, C., 476, 488 Durchon, M., 35, 86 Davis, H. C., 402, 403, 404, 405, 406, Durve, V. S., 434, 435, 439, 489 407,450,452,456,474,496 Dybern, B. I., 7, 8, 13, 22, 23, 26, 33, Davison, A. N., 219, 244 35, 37, 40, 42, 43, 44, 45, 62, 81, Dawson, A. B., 14, 86 86, 87 Deacon, G. E. R., 267, 328 Dynes, J., 476, 489 De Coque, J. V., 478, 488 Dziewiatkowski, D. D., 222, 245 Deevey, G. B., 164, 189, 195 Defant, A., 279, 286, 328 Defier, G. G. J., 208, 224, 244 Degens, E. T., 104,195, 213, 244 E Delff, C., 143,195 Delius, G., 477, 506 Earnest, R. L., 476, 484 De Marco, C., 215, 219, 220, 222, 243, Edie, S. E., 130, 199 Edlbacher, S., 212, 230, 248 244, 245 Denison, W. T., 460, 488 Edmondson, C. H., 362, 396, 401, 417, 419, 427, 430, 449, 463, 454, 456, Denton, C. A., 223, 249 459, 472, 476, 478, 480, 481, 489 Desohamps, P., 442, 488 Deshayes, G. P., 345, 357, 367, 370, Edmondson, W. T., 165,195 Edwards, C., 239, 245 381,429, 488 Devenish-Meares, R., 460, 488 Edwards, C. E., 477, 489 Diehl, M., 5, 6, 8, 26, 43, 46, 49, 81, 86 Eggers, A., 402, 487 Di Jeso, F., 206, 209, 250 Ekman, S., 56, 60, 62, 64, 65, 67, 69,87 Dilly, N., 22, 86 Eldjarn, L., 219, 220, 245 Dodd, J. M., 14, 86 Eldredge, L. G., 55, 69, 87 Dodson, A. N., 124, 203 Elias, L. A. P., 314, 315, 328 Dollfw, R. Ph., 472, 499 Elroi, D., 33, 46, 79, 80,82,87

’

616

AUTHOR INDEX

120, 122, 123, 124, 125, 126, 127, 128,196, 203, 311, 333 Ericson, L. E., 212, 245 Erlanson, E. W., 411, 476, 489 Ewetz, L., 215, 251

Fretter, V., 48, 49, 87, 390, 396, 402, 451, 490 Fries, A. A., 489 Frison, Ed., 480, 481, 490 Fromageot, C., 217, 218, 246 Fromageot,P., 205, 215, 217, 218, 238, 242, 243, 244 Frontier, S., 302, 328 Fuchs, H., 210, 246 Fuerst, R., 205, 211, 215, 217, 230, 242 Fukuota, J., 293, 329 Fulton, J. D., 139, 140, 200 Furnestin, J., 278, 285, 329 Fiirth, O., von, 205, 246

F

G

Ferguson, H., 481, 482, 504 Ferrara, R., 185,196 Fiadeiro, M., 103,196 Fischer-Piette, E., 35, 87 Fitzsimons, H. W., 478, 479, 480, 489 Fleming,R.H., 103,108,110,112,113, 145,196, 203, 260, 333 Fleminger, A., 302, 328 Flores, L. A., 314, 315, 316, 317, 328, 329 Florkin, M., 207, 208, 209, 210, 212,

Gabe, M., 388, 490 Gage, J., 26, 51, 87 Gaillard, J-M., 35, 87 Ganaparti, P. N., 290, 329, 341, 391,

El-Sayed, S. Z., 182, 183, 195 Elsey, C. R., 397, 419, 453, 485, 486 Embree, C . J., 456, 489 Emery, W. W., 477, 489 Emilsson, I., 264, 328 Emmel, V. M., 103, 201 Engel, R., 224, 245 Ennor, A. H., 209, 225, 227, 245 Eppley, R. W., 114, 115, 117, 118, 119,

226, 233, 234, 235, 236, 237, 240, 241, 243, 245, 246, 247, 445, 489 Floyd, N., 215, 217, 220, 249 Fogg, G. E., 103,196 Folkard, A. R., 278, 285, 330

Food and Agriculture Organization, 81, 87 Forsbergh, E. D., 276, 295, 315, 328 Fouque, G., 35, 87 Fox, M. H., 402, 487 Foxton, P., 279, 288, 289, 328 Foxworthy, F. W., 481, 489 Fraga, F., 207, 246 Franc, A., 35, 87 Fraser, C. M., 54, 87, 397, 489, 490 Frmer, D., 210, 246 Fraaer, J. H., 169, 196 Fraundorf, V. J., 302, 331 Fredericq, L., 208, 246 Fr6my, 205, 208, 211, 228, 252 Frerichs, F. T., 208, 251

419,490

Gardiner, A. C., 152, 196 Gareth Jones, E. B., 480, 507 Garner, D. M., 293, 329 Garrett, M. J., 240, 242 Geen, G. H., 151, 153, 161, 196,197 Gelder, N. M., van, 210, 239, 248 George, R. Y . , 69, 92 Georges, D., 14, 97 Gerking, S. D., 145, 196 Giese, A. C., 397, 431, 436, 437, 438, 485, 490, 507 Gifford, C . A., 440, 495 Gilmartin, M., 284, 334 Glaaer, O., 20, 46, 87 GIBmarec, M., 39, 87 Gmelin, L., 205, 252 Goering, J. J., 116, 182, 195, 196 Goldberg, E. D., 2, 3, 4, 46, 87, 90, 121, 196 Goldman, C. R., 294, 329 Gonggrijp, J. W., 480, 481, 491 Goodbody, I., 5, 7, 12, 21, 27, 28, 46, 48, 80, 87 Gordon, L. I., 103, 195 Gotto, R. V., 51, 88 Graham, A., 49,87,390,396,402,451, 490

616

AUTHOR INDEX

Graham, W., 476, 483 Grainger, E. H., 183, 184, 186,196 Grant, B. R., 116, 117,196 Grave, B. H., 26, 29, 88, 346, 390, 391, 394, 396, 401, 406, 416, 426, 444, 460, 469, 476, 490 Grave, C., 16, 16, 19, 20, 21, 46, 88 Gravely, F. H., 341, 490 Graziani, G., 47, 97 Graziani, M. T., 220, 244 Graves, J. R., 291, 327 Greedeld, L., 419, 424, 490 Greenfield, L. J., 407, 431, 434, 436, 436, 440, 441, 443, 446, 490, 491, 496 GrifFith, G., 32, 97 Grill, E. V., 109, 196 Gryder, R., 210, 239, 245 Gubin, F. A., 289, 330 Guillard, R. R. L., 113, 196 Guillen, 0. C., 316, 317, 329 Gulland, J. A., 309, 329 Gunter, G., 43, 81, 88 Gunther, E. R., 129, 197, 266, 268, 278, 284, 329 Gutierrez, M., 33, 36, 48, 88 Gutsell, J. S., 459, 491

H Hachey, H. B., 268, 329 Hafter, R. E., 208, 224, 244 Hall, G. E., 43, 81, 88 Hall, J. R., 279, 289, 294, 332 H m e r , W. H., 476, 481, 491 Hamilton, R. D., 104,196 Hancock, A., 357, 491 Hancock, D. A., 81, 88 Hansen, A. L., 163, 196 Hansen, V. Kr., 294, 332 Haq, S. M., 139, 197 Harant, H., 50, 62, 63, 64, 76, 81, 88 Harden Jones, F. R., 274, 329 Hardesty, W. P., 476, 491 Harding, J. P., 8, 88 Hardy, A. C., 129,197 Hargrave, B. T., 161, 163, 161, 197 Haxrington, C. R., 407, 441, 491

Harris, E., 108, 109, 126, 136, 141, 143, 144, 146, 146, 148, 149, 161, 162, 160, 162, 166, 189, 191, 192,197 Harris, H., 218, 219, 243 Hart, J. L., 460, 491 Hart, T. J., 268,269,260,279,286,329 Harting, P., 416, 446, 447, 463, 472, 491, 507 Hartley, J. B., 460, 491 Hartman, W. D., 48, 96 Hartmeyer, R., 66, 61, 62, 63, 68, 69, 71, 74, 76, 88, 89 Harvey,H. W., 106,113, 121,129,132, 136, 137, 138, 139, 164, 166, 170, 197, 270, 329 Hashimoto, M., 441, 491 Haslewood, G. A. D., 211, 227, 246 Hatanaka, M., 396, 403, 404, 406, 407, 449,460, 461, 463, 492 Hatschek, B., 402, 491 Haurowitz, F., 206, 246 Haven, N. J. D. T., 30, 89 Hayea, F. R., 270, 329 Hebant-Joder, A-M., 82, 89 Hecht, S., 2, 4, 89 Hedgpeth, J., 69, 89 Hedley, C., 60, 67, 89, 464, 472, 491 Heinle, D. R., 164,197 Heinrich, A. K., 304, 312, 329 Hellebust, J. A., 128,197 Henley, C., 402, 487 Hennacy, R. E., 406, 440, 496 Henry, E., 460, 491 Hentschel, E., 266, 267, 303, 306, 329 Heme, M., 208, 212, 229, 246 Herdman, W. A., 2, 68, 66, 69, 71, 72, 73, 76, 89 Herman, S. S., 129, 140, 144, 180, 181, 193,197 Herpin, R., 472, 491 Hess, N., 233, 244 Hess, R. W., 482, 503 Hesse, U., 477, 492 Hidaka, K., 260, 261, 264, 266, 291, 292, 322, 323, 329 Hidaka, T., 27, 90 Hill, C. L., 460, 476, 477, 481, 482, 492, 498, 501 Hill, D. K., 229, 246 Hillman, R. E., 208, 240, 246

617

AUTHOR INDEX

Hirai, E., 6, 12, 13, 89 Hisaw, F. L., 14, 89 Hisaw, F. L., Jr., 14, 86, 89 Hoag, S . W., 460, 492 Hobby, A. S . , 417, 492 Hobson, G. E., 209, 227, 246 Hochman, H., 208, 210, 244 Hoech, 478, 492 Hoeven, J. V., 447, 492 Hoffman, H., 49, 89 Hoggarth, K. R., 366, 492 Holbrook, F. W. D., 481, 492 Holderness, D., 476, 492 Hollaender, A., 104, 201 Holmea, R. W., 267, 296, 329 Holm-Hansen, O., 106, 113, 114, 116, 126, 127, 128,197, 203 Holtfreter, J., 210, 246 Holtz, F., 208, 212, 242 Hooper, R.B., 477, 492 Hope, D. B., 214, 218, 243, 247 Hopkins, A. E., 469, 492 Horn, E. F., 480, 492 Houghton, D. R., 36,79, 80, 81,89, 98 Howard, C. E., 210, 239, 251 Howard, G . V., 276, 277, 278, 332 Howe, W., 477, 492 Hoyle, G., 4, 89 Hughes, G. C., 468, 492 Hunt, A. M., 476, 492 Hunt, G. M., 482, 492 Huntsman, A. G., 26, 27, 89 Hurley, D. E., 397, 426, 426, 428, 476, 492, 503 Hutchins, L. W., 8, 90, 462, 503 Hutohinson, G. E., 319, 321, 329 Huus, J., 13, 66, 62, 63, 64, 81, 90 Hyman, L. H., 471, 492

I

Ichikawa, E., 208, 251 Ikeda, I., 367, 469, 492 Illg, P. L., 60, 61, 90 Ilsley, A. B., 481, 492 h i , T., 396, 403, 404, 406, 407, 449, 460, 461, 463, 493

Iredale, T., 364, 359,426,428,443,464, 462,463,476,481,482, 493, 494, 508 hie, Y., 208, 210, 212, 251 Isham, L. B., 401, 403, 404, 406, 409, 424, 426, 467, 493 Iterson, G. van, 478, 479, 480, 493 Ito, K., 212, 239, 247 Ivanenkov, V. N., 289, 330 Ivanova-Kazas, 0. M., 30, 51, 90 Ivley, V. S., 304, 330

J Jacobsen, J. G., 211,214,218,219,221, 222, 223, 247 Jaeger, M. F., 481, 493 Jamakawa, M., 208, 210, 212, 251 Janka, R., 207, 210, 212, 241 Jansen, B. C. P., 207, 247 Japan, Science Council, 298, 330 JesviS, E. R., 481, 493 JarVis, G. E., 478, 493 Jaxvis, J.,460, 481, 493 Jawed, M., 147, 161, 162,197 J a y m m m , R., 420, 503 Jefferies, R. P. S., 22, 90 Jeffries, H. P., 131, 197 Jeffreys, J. G., 363, 429, 449, 461, 474, 493 Jelley, J. F., 476, 493 Jellkck, B., 206, 207, 209, 210, 212, 213, 247 JenningS, J. B., 60, 90 Jensen, E. A., 294, 332 Jeuniaux, C., 207, 208, 209, 210, 212, 226, 233, 234, 236, 236, 237, 243, 245, 246, 247, 446, 493 Johmeck, R., 131,199 Johanna, R. E., 102, 131,. 147, 164, 161, 192,197, 204, 209, 239, 252 Johnson, A. A., 476, 477, 484 Johnson, C. H., 417, 493 Johnson, M. W., 103, 203, 397, 416, 419, 425, 460, 493 Johnson, R. A., 364,369,426,428,442, 443, 464, 466, 462, 463, 476, 478, 481, 482, 493, 494, 508 Johnson, T. W., 468, 494 J o m , E., 474, 494

518

AUTHOR INDEX

Jones, E. B. G., 459, 494 Jones, L. W. J., 425, 475, 487 Jones, M. M., 279, 289, 294, 332 Jones, N. S., 42, 90 Jones, P. G . W., 278, 285, 286, 330 Jones, W. A., 476, 494 Jordan, R.,317, 334 Jorgensen, C. B., 2, 3, 4, 90, 130, 132, 197, 402, 404, 494 Joseph, J., 295, 315, 328 Joshimura, K., 208, 210, 212, 251 Jost, E., 3, 84 Jungersen, H., 474, 494

K Kabanova, Yu. G., 290, 295, 297, 330 Kamshilov, M. M., 303, 330 Kanai, M., 205, 253 Kanatani, H., 27, 90 Karande, A. A,, 396, 406, 407, 458, 494 Karsten, 207, 247 Kasi, A., 210, 239, 245 Kassab, R.,227, 247 Kawahara, T., 79, 80, 90 Kelly, A., 207, 208, 211, 228, 247 Kelly, A. C., 180, 193 Kelly, J. A., 34, 81, 86 Kemp, S., 52, 91 Kennedy, 0. D., 140, 200 Kennon, C. W., 476, 494 Kermack, W. O., 210, 212, 213, 240,246, 247 Kester, D. R.,105, 198 Ketchum, B . H., 107, 108, 110,

298,

444,

214,

117, 121, 122, 123, 124, 128, 144, 145, 152, 155, 161, 162, 166, 173, 174, 175, 176,198, 201, 267, 330 Khromov, N. S., 294, 302, 327, 330 Kieny, M., 14, 97 Kikuchi, T., 34, 91 Kindle, E. M., 415, 448, 494 Kinne, O., 447, 452, 494 Kirk, P. W., 458, 459, 494, 495 Kirkbride, W. H., 430, 451, 475, 476, 481, 495, 501

Kittredge, J. S., 206, 207, 209, 210, 212, 213, 247 Knaben, N., 13, 43, 44, 91 Knauss, J. A., 263, 288, 330 Knox, G. A., 55, 64, 65, 67, 68, 91 Knudsen, J., 62, 90 Kobayashi, S., 435, 481, 497, 501 Koblentz-Mishke, 0 . I., 291, 294, 296, 330 Koechlin, B. A., 208, 223,224, 230,247 Kofoid, C. A., 355, 396, 401, 419, 425, 430, 451, 453, 495 Kohlmeyer, J., 409, 413, 458, 485, 495 Kojima, Y., 208, 248 Kolar, Z., 82, 98 Komarovsky, B., 8, 23, 33, 46, 79, 80, 82, 87, 91 Konosu, S., 207, 248 Kooy, C., 478, 479, 495 Korringa, P., 3, 91, 337, 495 Kossel, A., 212, 230, 248 Koszalka, T. R.,210, 246 Kott, P., 5, 15, 16, 18, 39, 55, 59, 64, 65, 66, 67, 69, 71, 72, 73, 74, 76, 77,91 Kramp, P. L., 415, 426, 450, 481, 495 Kravitz, E. A., 210, 239, 248 Krishnaswamy, S., 397, 433, 490, 508 Krogh, A., 130,198, 229, 248 Kromphardt, H., 233, 248 Krukenberg, C. F. W., 205, 207, 208, 248 Kuenzler, E. J., 121, 122, 123, 124, 128,198 Kuffler, S. W., 210, 239, 245, 248 Kuriyama, M., 212, 248 Kurtz, A. C . , 207, 209, 212, 225, 231, 248 Kusakabe, H., 208, 248 Kutscher, F., 208, 212, 242

L Laevastu, T., 290, 327 Lafargue, F., 15, 36, 37, 47, 91 La Fond, E. C., 290, 298, 330 Lakshmana Rao, M. V., 341, 490 Lambert, C. C., 13, 91

AUTHOR INDEX

519

Loosjes, F. E., 478, 479, 506 Lambert, G., 20, 26, 46, 50, 91 Lopez-Capont,M., 207, 246 Lamy, E., 354, 495 Loppens, K.,479, 480, 496 Lance, J. R.,129, 201 Landva, A. J., 205, 211, 215,217, 230, Lovegrove, T.,304, 331 Lowe, I. P.,223, 224, 249 242 Lane, C. E., 206, 212, 248, 345, 366, Lowry, J. K.,43, 85 386, 401, 406, 406, 407, 409, 426, Luck, J. M., 207, 209, 212, 225, 231, 248 431, 434, 436, 440, 441, 443, 444, Lutzen, J., 7, 10, 51, 52, 62, 64, 84, 92 469, 490, 495, 496 Lynch, M. P.,233, 249 Lane. R. K.,260, 273, 333 Lange, R.,206,207,212,215,233,236, Lynch, W.F.,20, 92 Lynn, R. J., 272, 273, 280, 281, 282, 237, 238, 248 331 Larkins, H.A.,273, 316, 324, 326 Lasker, R.,129, 166,169,198,306,330, 431, 434, 436, 443, 496 M Laubier, L., 41, 91 McAllister, C. D., 107, 113, 126, 128, Lawrence, J., 397, 490 193,199,267, 326,331 Lay, S., 33, 35, 48, 88 McBlair, W., 3, 4, 46, 87 Lazet, F.,446, 489 Lazier, E. L., 346, 368, 367, 372, 374, Macallum, A. B.,238, 249 401, 419, 425, 430, 441, 451, 453, McCarthy, J. J., 115, 118, 119, 120, 124, 125,196 495,496 Lebour, M.V., 129, 132, 136, 137, 139, McCosh, G. K.,15, 20, 21, 88 154, 197, 270, 329, 397, 401, 404, McDonald, P.M., 50, 96 Macdonald, R.,130,198 496 McDougall, K.D., 6, 27, 92,417, 497 Le Brasseur, R. J., 139, 140, 200 McEwen, G. F.,256, 266, 331 Lee, A. J., 279, 289, 330 474,496 Lees, H.,210, 212, 213, 214, 240, 246, MacGillivray, W., MacGinitie, G. E., 2, 3, 34, 53, 63, 92 247 MacGinitie, N., 53, 92 Lehmann, 462, 496 McGlone, R. G., 456,497 Letellier, A., 207, 248 M’Gonigle, R. H.,448, 463, 456, 466, Levine, E.P.,6, 15, 20, 21, 91 481, 497 Levinson, L. B., 469, 496 McGowan, J. A., 302, 331 Levy Salvador, P.,415, 461, 496 MacMin, L. J., 223, 249 Lewis, J. R.,33, 45, 91 Lewis, P. R.,208, 210, 228, 229, 230, McIntosh, W.C., 472, 497 MacIsaac, J. J.,117, 119, 120, 121,198 248 Mackenzie, A.C., 448,460, 496 L’Hmdy, J.-P., 8, 9, 92 Mackintosh, N.A., 64, 92 Lindberg, B.,212, 239, 248, 249 Linford, E.,143,148,151,152,198,201 McLaren, I. A.,171, 199, 303, 331 Linn, R.J., 114,115,126,127,128,203 MacLean, J. D.,476, 477,496 McNeill, F.A.,354, 359, 426,428, 443, List, P.H., 206, 227, 242 454, 462, 463, 476, 481, 482, 493, Liu, D. L., 446, 496 494, 508 Lloyd, I.J., 294, 295, 296, 300, 330 McQuaid, H. S., 476, 477, 497, 508 Lo Bianco, S.,8, 9, 23, 92 McWhinnie, M. A., 131,199 Longard, J. R.,258, 331 Madgwick, J., 115, 196 Longhurst, A. R.,274, 331 Loosanoff, V. L., 91, 92,402,403,404, Madsen, F.J., 5, 92 406, 406, 407, 449, 450, 452, 466, Mmda, Y.,207, 248 Mahnken, C. V. W.,295, 296, 328 474, 496

520

A m O R INDEX

Makisumi, S., 206, 249 Mal’m, E. W.,477, 496 Manwell, C., 162, 198,386, 497 Maraglino, G.A.,82, 92 Mariot, A., 466, 497 M m , J. C., 309, 316, 327, 331 Marshall, H.B.,460, 491 Marahall, J. T.,474, 477, 497 Marahall, S.M., 129, 132,133, 134, 137, 138, 139, 140, 141, 143, 144, 146, 147, 148, 149, 161, 162, 163, 154, 156, 166, 167, 168, 169, 162, 163, 164, 166, 166, 167, 169, 170, 193, 194, 198, 199, 303, 304, 331 Martell, A. E., 103, 202 Martens, Ed. von, 474, 497 Martin, J. H.,129, 161, 152, 166, 169, 160, 162, 187,199 Martin, W.G.,223, 224, 249 Maat, S. O.,19, 92 Mesurekar, V. B., 346, 366, 366, 368, 484 Matsumoto, W. M., 323, 331 Matthews, H.M., 161, 163, 154, 201 Mattos, F.D.,476, 481, 501 Mattox, N. T.,469, 497 Mauchline, J., 130,199 Mawatari, S., 416, 430, 441, 448, 449, 460,481, 497 May, E., 364, 360, 497 Mayfield, P.B.,477,497 Mazeika, P.A.,291, 293, 331 Medes, G.,216, 217, 220, 249 Mell, C. D.,478,479, 480, 503 Mendel, L.B.,207, 211, 249 Menegaux, A., 384, 497 Mensah, M. A., 302, 331 Menzel, D.W.,103, 174, 178, 179, 180, 181, 182, 195, 196, 199, 202, 312, 333 Menzies, R. J., 69, 92, 406,497 Mequaid, H.S., 476,477,484 Methven, C. W.,482, 497 Meyere, 8. P.,469, 497 Miohaelsen, W.,69, 60, 66, 67, 68, 69, 73, 74, 76, 92,93 M”’ ,R., 5, 49, 93

Millar, R. H., 2, 3, 4, 6, 6, 8, 9, 10, 11, 12, 14, 16, 16, 18, 19, 21, 22, 23, 26, 26, 28, 30, 33, 36, 37, 39, 40, 46, 60, 61, 62, 66, 66, 67, 68, 69, 71, 72, 73, 74, 76, 77, 80, 81, 89, 93, 94 Millard, N., 8, 23, 94 Miller, L.,210, 246 Miller, R. C., 345, 353, 364, 366, 360, 366, 366, 367, 396, 397, 401, 416, 419, 425, 426, 430, 434, 441, 443, 460, 461, 453, 467, 476, 477, 484, 486, 488, 493,495,497, 498 Min, H.S., 161, 163, 164, 201 Miraglia, R.J., 223, 224, 249 M i t o h e l l - h e s , B. A,, 298, 331 Miyazaki, I., 404,415, 498 Mobius, K.A.,481, 498 Mold, J. D.,207, 250 Molinier, R.,42, 83 Moll, F., 364, 369, 430, 461, 472, 474, 478, 479, 498 Mondovi, B., 219, 220, 222, 249 Mondovi, P.B.,220, 243 Money, W.T.,478,480, 498 Monniot, C., 6,6,36, 36, 37, 38,40,41, 42, 43, 44, 46, 46, 52, 54, 62, 69, 72, 73, 76, 87, 94 Monniot, F.,6, 6,38, 64,69,72, 73,76, 94 Monod, T.,472, 498 Monod, Th., 362, 499 Montanus, A.,478, 479, 499 Moore, B.,130,199 Moore, D.D.,466, 494 Moore, H.B.,449, 462, 460, 499, 506 Moore, S., 146, 199 Morgans, J. F.C., 33, 94 Morizawt~,K.,208, 249 Morrison, J. F.,209, 226, 227, 246 Morton, B. S., 366, 368, 372, 381, 499 Morton, J. E., 366, 376, 499 Moseley, H.N.,72,94 Mosti, R.,216, 244 Moyle, V., 162, 195 Mukai, H.,31, 94 Mullin, M. M., 129, 137, 139, 163, 164, 166, 171,199, 200 Mullins, L.J., 230, 249 Murphy, J., 136,140,200

521

AUTHOR INDEX

Murthy, V. S. R., 290, 329 Myrland, P., 289, 332

Nomejko, C. A., 449, 496 Norris, E. R.,441, 498

0 N

Odense, P. H., 206, 227, 244 Odo, K.,208, 251 Ogawa, K.,260,261,264,291,292,322, 323, 329 Ohsima, Y.,476, 501 Oh,A., 62,65, 58, 74, 75, 95 Oka, H., 28, 29, 31, 95 Okmaki, K.,435, 501 Okuda, Y.,208, 210, 212,249 Oliver, W.R.B., 33, 95 Olumucki, A.,226, 252 Omon, M.,129, 159,193 Onoma, K.,441, 491 Onosaka, M.,27, 90 Oord, A,, van den, 228, 249 Organization for Economic Co-operation end Development, 80, 95 Orr, A. P., 129,132,133,134,138,141, 144, 163, 154, 165, 167, 198, 199, 200, 303, 304,331 Orren, M. J., 286, 332 Orton, J. H., 2, 8, 23, 26, 95, 415, 450, 476, 501 Osburn, R.C., 474, 506 Osler, E.,452, 501 Ouchi, S., 207, 220, 249, 251 Owen, G.,419, 424,467,501 Ozrtki, Y.,357,469, 492

Nagabhushanam, R., 341, 388, 391, 396, 401, 406, 410, 414, 415, 419, 427, 436, 438, 448, 450, 453, 454, 457,458,459,463,490,499 Naidu, J. R., 290,327 Nair, N. B., 79, 95, 341, 345, 353, 354, 355, 356, 357, 358, 359, 360, 365, 366, 367, 368, 373, 374, 378, 379, 381, 382, 383, 384, 385, 386, 387, 388, 391, 397, 399, 400, 402, 403, 404, 405, 406, 409, 410, 412, 413, 414, 415, 416, 419, 426, 427, 431, 434, 442, 443, 446, 447, 448, 450, 451, 452, 454, 460, 461, 462, 463, 465, 466, 467, 468, 469, 473, 474, 476, 481, 483, 484, 499, 500, 505 N h i , Z., 143, 144, 200 N a b m a , H.,315, 322, 631 Nakamura, S., 212, 251 Nakauchi, M.,29, 30, 95 Nakazawa, K.,404, 500 Nanji, D. R., 480, 500 Nathansohn, A.,265, 331 Naylor, E., 25, 44, 95 Neave, F.,397,415, 500 Needham, A.E., 152, 200 Needler, A.B.,450, 475, 501 Needler, A.W.H., 460, 475, 501 Negus, M.R. S., 207,249 P Neiley, R.M.,476,481, 501 Paffenhofer, G-A., 130, 164, 165, 200 Nellen, W.,296, 331 Nelson, T. C., 406, 415, 448, 450, 469, Palekar, V. C., 341, 501 Pdombi, A.,469, 502 471,475, 501 Panikkax, N. K., 341, 502 Neunes, H.W.,129, 200 Pant, R.,206,242 Newell, B. S., 147, 195 Parenzan, P., 34, 42, 95 Nicholas, D. J. D., 115, 200 Nicholls, A. G.,138, 163, 167, 199, 200 Park, K.,111, 200 Parker, P. D. M., 103,193 Nicholson, G.F., 461, 501 Parsons,T.R.,107,112, 113, 126, 128, Nicholson, G.T.,477, 501 139, 140, 164, 193, 199, 200, 203, Nicholson, H.F.,267, 270, 328 267, 326, 331 Nicoll, P. A.,20, 88 Patriok, H., 223, 224,249 Nielsen, E. S., 294, 331, 332

622

AUTHOR INDEX

Patullo, J. G., 260, 273, 333 Pavlov, V. Y., 302, 332 Pavlova, E. V., 143, 169, 170, 171, 200 Pearson, P. B., 223, 249 Pease, A. K., 279, 289, 294, 332 Peck, E. J., 217, 224, 250 Pelseneer, P., 502 Pendsey, 5. S., 396, 494 Peres, J-M., 23, 26, 34, 36, 42, 54, 55, 60, 62, 95, 96 Perras, J. P., 122,198 Pessin, L. J., 474, 502 Petersen, M. B., 207, 233, 250 Petipa, T . S., 169, 170, 171, 200, 201 Pfleger, K., 3, 84 Picard, J., 33, 42, 83, 96 Pickard, E. A., 469, 502 Pihl, A., 219, 220, 245 Poblete, M. J., 461, 502 Polk, P., 8, 9, 20, 36, 96 Pomeroy, L. R., 151, 153, 154, 165, 201,202 Pongolini, G-F., 129, 200 Pope, E., 33, 86 Pope, E. C . , 50, 96 Porcellati, G., 210, 250 Posner, G. S., 278, 285, 332, 407, 431, 434, 436, 443, 495 Potter, D. D., 210, 239, 245, 248 Potts, F. A., 345, 368, 372, 373, 374, 396, 441, 443, 445, 460, 502 Potts, W. T . W., 207, 208, 232, 250 Powell, H. T., 33, 45, 91 Pradel, L. A., 209, 220, 225, 226, 227, 247, 250, 252 Pratt, D. M., 107, 185, 186, 187, 201 Prema, S., 396, 406, 407, 444, 458, 494 Prenant, M., 36, 96 Pringle, E., 206, 212, 248 Provasoli, L., 129, 201 Prudden, T . N., 477, 502 Prudon, L., 415, 461, 496 Prytherch, H. F., 459, 502 Purchon, R. D., 345,357,368,365,366, 368, 369, 370, 371, 376, 378, 380,

502 Putnam, J. W., 415, 456, 502 Putter, A., 130, 201 Pytkowicz, R. M . , 105, 111, 198, 201

Q Quatrefages, A. de, 345, 365, 370, 402, 502 Quayle, D. B., 397, 399, 404, 406, 419, 426, 443, 450, 451, 502

R Raben, E., 143, 193 Rae, B. B., 48, 50, 96 Raja, B. T . A., 6, 12, 79, 96 Rajagopalaiengar, A. S., 340, 454, 503 Rakeatraw, N. W., 103, 104, 192, 201, 203 Ralph, P. M., 397, 425, 426, 475, 503 Ramage, W. D., 477, 503 Ramamirthan, C. P., 420, 503 Rama Sastry, A. A., 289, 332 Rancurel, P., 362, 388, 404, 406, 424, 472, 490, 503 Randell, J. E., 48, 96 Rathbun, R., 474, 503 Rathke, J., 472, 503 Raymont, J. E. G., 143, 144, 148, 151, 152, 201, 433, 503 Raymont, J. K. B., 143, 144, 201 Read, K. R. H., 386, 503 Read, W. O., 224, 230, 250, 253 Record, S . J., 478, 479, 480, 482, 503 Redeke, H. C., 415 Redfield, A. C., 106, 108, 109, 110, 144, 152, 155, 177, 201, 293, 332, 462, 503 Redgrave, G. R., 463, 472, 503 Redi, F., 384, 503 Redikorzev, V., 76, 96 Rees, C. B., 404, 503 Rees, K. R., 209, 227, 246 Reeve, M. R., 169, 201 Reid, J. L., Jr., 257, 268, 263, 267, 268, 269, 270, 272, 278, 284, 291, 302, 303, 311, 315, 316, 332, 334 Reid, R. G. B., 371, 504 Relini, G., 34, 79, 80, 96 Renn, C. E., 192, 203 Renouf, L. P. W., 47, 96 Reuter, J. H., 104, 195 Reyne, A., 479, 504

623

AUTHOR INDEX

Riabchikov, P. I., 448, 504 Richards, A. P., 477, 504 Richards, B. R., 415, 426, 504 Richards, F . A., 107, 108, 109, 110, 144, 152, 155, 196, 201, 202, 272, 278, 293, 332, 333 Ricketts, E. F., 61, 96 Ridewood, W. G., 376, 379, 380, 504 Riegel, B., 207, 250 Riggs, T . R., 233, 244 Riley, G. A., 102, 107, 108, 109, 126, 129, 137, 138, 139, 141, 143, 144, 145, 152, 166, 187, 188, 189, 191, 197, 202, 267, 326, 332 Riley, J. P., 104, 131, 135, 140, 146,

153,193,194, 200, 202 Ritter, W. E., 5, 69, 71, 72, 74, 96 Rivera, IT., 474, 478, 479, 504 Roberts, E., 206, 207, 209, 210, 212, 213, 223, 224, 247, 249 Robertson, J. D., 207, 208, 230, 250 Robin, Y., 206,209,220,224,225,226, 227, 250, 252 Robinson, M. K., 279, 289, 295, 296, 334 Robinson, R. J., 153, 196 Roch, F., 340, 354, 359, 363, 364, 365, 385, 401, 424, 430, 443, 448, 453, 454, 459, 461, 467, 467, 471, 472, 474, 498, 504 Roche, J., 206, 209, 220, 224, 225, 227, 250, 252 Rochford, D. J., 288, 290, 332 Roden, G. I., 258, 272, 278, 293,

449, 469, 226,

316,

332 Rodrigues, S. de A., 60, 96 Roe, D. A., 208, 210, 250 Roessler, S. W., 476, 504 Rogers, J. N., 115, 118, 119, 120, 124, 125,196

Rojas, B. de Mendiola, 311, 333 Roonwal, M. L., 340, 474, 504 Rose, S. M., 13, 96 Roughley, T . C., 476, 481, 504 Roule, L., 2, 97 Rummel, W., 3, 84 Runnstrom, S., 8, 23, 25, 44, 97 Russell, F . S., 129, 132, 136, 137, 139, 154,197, 270, 318, 329, 332 Rust, 5. F., 481, 482, 504

Ryhage, R., 228, 249 Ryther, J. H., 103, 117, 174, 178, 179, 180, 181, 182, 195, 199, 202, 203, 279, 289, 294, 332

S Sabbadin, A., 8, 9, 23, 27, 29, 30, 31, 33, 44, 47, 97 Salfi, M., 30, 53, 97 Salkowski, E., 226, 250 Sanada, K., 208, 210, 249 Sanders, H. L., 34, 97 Santhakumari, V., 469, 471, 504, 505 Saraswathy, M., 345, 355, 356, 357, 358, 365, 368, 373, 374, 379, 381, 383, 384, 386, 287, 397, 401, 412, 419, 428, 431, 443, 454, 456, 505 Sarlet, H., 212, 233, 243 Sato, R., 396, 403, 404, 406, 407, 449, 450, 451, 453, 492 Satomi, M., 155, 202 Savilov, A. I., 36, 97 Scandurra, R., 220, 244 Schaefer, M. B., 267, 276, 277, 278, 279, 289, 295, 296, 329, 332, 334 Scheer, B. T., 7, 23, 80, 97 Sohellenberg, A., 50, 97 Schelske, C. L., 294, 325, 334 Scheltema, R. S., 415, 425, 446, 451, 453, 456, 505

Schinske, R. A., 3,98 Schlesinger, R. W., 210, 239, 251 Schmidt, C. L. A., 207, 251 Schmidt, F., 471, 505 Schmidt, H., 474, 478, 485 Schmidt, R. W., 206, 227, 244 Schmitt, O., 228, 242 Schoberl, A., 220, 251 Schoffeniels, E., 210, 237, 238, 240, 241, 246, 251 Schott, G., 255, 332 Schram, E., 205, 226, 251 Schulze, B., 401, 443, 477, 485 Schwartz, F . J., 32, 97 Schwartz, I., 8, 23, 91

I

624

AUTHOR INDEX

Schweiger, R. G., 212, 239, 251 Scott, C. W., 416,505 Searles, J. W., 448, 461, 487 Sebastian, V. O., 12. 19, 21. 97 Seifen, E., 3, 84 Sekine, T., 208,251 Sellius, G., 346, 446, 453, 474, 478, 505 Sengel, P., 14, 97 Sentz-Braconnot, E., 26, 79, 81, 98 Shackell, L. F., 477, 506 Shackleton, P., 476, 505 Shannon, L. V., 286, 332 Sharp, J., 106,197 S h w , E. H., 230, 253 Shaw, J., 234, 236, 237, 251 S h w , N. F., 104,195 Shaw, W. S., 480, 500 Shibuya, S., 207, 220,251 Shimada,B. M., 267, 295, 329 Shimishi, K., 129, 201 Shuffleton, 5. L., 477, 505 Shuehkinct, E. A., 171, 202 Sigerfoos, C. P., 346, 361, 363, 366, 367, 368, 369, 360, 366, 367, 372, 373, 376, 379, 380, 381, 383, 384, 386, 388, 390, 396, 401, 402, 404, 406, 416,426, 460, 461, 505 Sillen, L. G., 103, 106, 202 Simonsen, D. G., 206, 207, 209, 210, 212, 213, 214, 247 Simpson, J. G., 277, 333 Simpson, J. W., 206, 206, 207, 208, 209, 210, 212, 213, 219, 221, 231, 251 Simsi, R. W., 469, 495 Sivertz, C., 238, 249 Skerman, T. M., 12, 79, 80, 98 Slinn, D. J., 49, 98 Slobodkin, L. B., 306, 306, 333 Sluiter, C. P., 62, 68, 67, 69, 98 Gmayada, T. J., 186, 202, 277, 333 Smith, D. G., 212,253 Smith, E. A., 474, 505 Smith, F. G. W., 424, 426, 467, 469, 488, 493 Smith, H. G., 64, 98 Smith, J., 346, 390, 394, 490 Smith, L. H., 211, 214, 218, 219, 221, 222, 223, 247 Smith, M., 467, SO5

Smith, M. J., 49, 98 Smith, M. L., 401, 428, 505 Smith, R. L., 260, 272, 273, 286, 326, 333 Smollett, T., 448, 505 Smout, P.S., 476, 505 Sokolov, V. A., 294, 327 Sokolska, M. N., 79, 98 Soloreano, L., 103, 106, 114, 117, 122, 196, 202, 203 Somme, 0. M., 419, 505 Sommer, H., 207, 250 Somogyi, M., 442, 505 Sarbo, B., 216, 251 Spaeth, D. G., 223, 224, 249 Spmth, J. P., 174, 180,199 Specht, R. C., 460, 506 Spengler, L., 474, 506 Spiegel, 5. L., 291, 327 Spoon, W., 478, 506 Spooner, G . M., 460,479, 506 Springer, V., 424, 426, 457, 493 Squire, H. E., 476, 481, 501 Sreenivaaan, V. V., 436, 437, 506 Srinivasagam, R. T., 143, 144, 201 Staedeler, C., 208, 251 Stander, G . H., 286, 333 Stanger, D. W., 207, 250 Stauber, L. A., 461, 506 Stearns, C. R., 326, 326 Steel, T., 466, 506 Steele, J. H., 140, 192, 306, 308, 310, 312, 333 Stefano, M., de, 82, 92 Stefansson, U., 107, 110, 202,272,278, 333 Stein, W. H., 146,199 Stempel, 0. A., 476, 506 Stephens, G. C., 3, 98, 131, 203 Stephens, K., 112, 113, 126, 128, 193, 199, 200, 267, 326 Stephenson, T. A., 68, 98 Stevens, T. M., 210, 239, 251 Stew&, W. D. P., 128, 203 Steyermark, A., 433, 506 Stimpson, W., 474, 506 Stirpe, F., 219, 220, 222, 243 Stommel, H., 268, 264, 279, 288, 289, 326, 332, 333. 334

I

, 1 I

626

AU!l'EOB INDEX

Storm Buysing, D. J., 415, 446, 447, 472, 507

Strickland, J. D. H., 103, 106, 107, 112, 113, 114, 116, 122, 126, 127, 128, 130, 164, 193, 196, 197, 199, 200, 202, 203, 267, 311, 326, 326, 331, 333 Strohal, P., 82, 98 Stubbings, H. G., 36, 79, 80, 98 Subrahmanyan, R., 289, 333 Sugino, K., 208, 251 Sugiura, Y., 112, 203 Sullivan, C. M., 403, 404, 450, 506 Sumner, F. B., 474, 506 Sutcliffe,W. H., Jr., 105, 130, 142,193, 197, 203 Suzuki, U.,208, 210, 212, 251 Sverdrup, A., 219, 245 Sverdrup, H. U., 103, 185, 203, 268, 259, 260, 264, 278, 333 Swallow, J. C., 258, 279, 288, 289, 333, 334

T Tabachnick, M.,215, 251 Tabechian, H., 218, 244 Tack, a. W., 480, 483 Taft, B. A., 288, 330 Tag&, M., 212, 251 T E ~ ~S.,E 208, , 220, 252 Taxasov, N. I., 448, 474, 475, 506 Tarver, H., 215, 251 Tatro, C. P., 477, 506 Taylor, K. M., 3, 4, 46, 87 Teesdale, C. H., 477, 506 Tentori, L., 220, 243, 249 Thr~l-Tun,103,196 Theilacker, G. H., 129, 198 Theophrastus, 478, 479, 506 Thiem, N. V.,206, 209, 224, 226, 226, 252

Thoai, N. van, 206, 209, 220, 224, 225, 226, 227, 250,252

Thoai, N. V.,227, 247 Thomas, L.L.,218, 219, 247 Thomas, W. H., 122,123,124,196,203 Thompson, H., 34, 48, 66, 61, 98 Thompson, T. E., 49, 98

Thoorn, N. A. M. van den, 479, 506 Thornborough, J. R., 43, 85 Thorrington-Smith,M., 298, 333 Thorson, G., 45, 98, 405, 451, 506 Thrailkill, J. R., 266, 282, 283, 304. 333, 334

Tibbitts, S., 105, 156, 193 Tiedemann, F., 205, 252 Tierney, J. Q., 366, 401, 403, 404, 406, 409, 440, 493, 496

Tokioka, T., 60, 54, 65, 56, 58, 63, 64, 81, 99

Tooms, J. S., 290, 318, 321, 334 Townsend, C. H., 319, 321, 334 Townsley, P. M., 446, 496 Tranter, D. J., 301, 334 Trason, W. B., 14, 16, 16, 21, 64, 99 Trueman, E. R., 366, 483, 492, 507 Truitt, R. V., 415, 425, 446, 461, 453, 456, 505

Trussel, P. C., 477, 480, 507 Teubab, B., 6, 13, 89 Tubrtki, K., 468, 507 Tucker, J. S., 397, 436, 490, 507 Tully, J. P.,435, 460, 507 Tungate, D. S., 325, 327 Turner, R. D., 337, 338, 346, 356, 357, 360, 376, 401, 446,

362, 363, 364, 365, 367, 368, 379, 380, 381, 385, 389, 399, 424, 426, 429, 430, 431, 444, 447, 507 Tub, J., 82, 98

U Upton, J., 476, 507 U.S. Navy ' H y d r o g ~ ~ @Office, ~ i ~ 280, 286, 334

Usui, M.,28,29,95

V Vaccaxo, R. F., 103, 104, 107, 108, 117, 173, 174, 175, 180, 198, 202, 203 Valder, G., 478, 507 Valenciennes, A., 206, 208, 211, 228, 252

626

AUTHOR INDEX

Van Buren, J. D., 460, 486 Vanin, S. I., 474, 507 Van Name, W. G., 47, 58, 60, 61, 63, 66, 71, 72, 73, 74, 75, 81, 82, 99 Van Oordt, J. W. L., 415, 446, 447, 472, 507

Van Slyke, E., 401, 419, 425, 430, 451, 453,495

Vmu, B. S., 397, 490 Venkataraman, R., 434, 507 Vernay, S., 29, 99 Verrill, A. E., 69, 99, 474, 507 Villanueva, R., 317, 334 Vinogradov, A. P., 82, 99, 143, 203, 307, 312, 334, 431, 434, 507

Vinogradova, N. G., 64, 69, 74,99 Vinogradova, Z. A., 143, 203 Viswanatha Sarma, A. H., 289, 333 Von Baumhauer, E. H., 507 von Brand, T., 192, 203 Vonk, H. J., 227, 252, 445, 507 Von Schrenk, H., 457, 463, 476, 507 Vrolik, W., 415, 446, 447, 472, 507

w Walker, T. J., 121, 196 Wainer, A., 215, 252 Walden, C. C.,446, 477, 496, 507, 508 Walker, D. M., 205, 211, 252 Walker, H. W., 476, 477, 484, 508 Walne, P. R., 407, 508 Walsh, H. D., 467, 481, 508 Warren, B., 258, 279, 288, 289, 334 Wmserman, R. H., 154, 203 Watanabe, H., 31, 95 Watanabe, K., 208, 251 Watkins, J. C.,239, 244 Watson, C. J. J., 428, 454, 463, 508 Watson, T., 207, 250 Watson, W., 425, 475, 487 Wattenberg, H., 156, 204,255,267,329 Waugh, G. D., 81, 99 Webb, D. A,, 228, 252 Webb, K. L., 131, 147, 197, 204, 209, 239, 252, 253

Wedekind, H., 461,462, 508 Weel, P. D. van, 445, 508 Weinstein. F.. 39. 99 Weiss, C. M., 12, 79, 80, 100, 462, 508

Weiss, H. F., 476, 508 Welty, J. D., 224, 230, 250, 253 Welty, J. D., Jr., 230, 253 Werner, B., 2, 3, 100 Werner, E., 2, 3, 100 Weston, M. O., 208, 250 Westwood, J. O., 481, 485 Whisenand, A., 121,196 White, F. D., 415, 453, 508 White, K. M., 387, 508 Whitley, E., 130, 199 Whittaker, J. R., 20, 100 Whittingham, D. G., 13,100 Wickberg, B., 212, 239, 253 Wikholm, D. M., 207, 250 Wilbur, K. M., 431, 508 Williams, P. M., 113, 197 Wilson, C. B., 472, 508 Wilson, D. F., 129, 204 Wilson, D. P., 405, 508 Wingo, W. J., 217, 218, 242 Wolfe, D. A,, 294, 325, 334 Wolff, T., 69, 100 Wood, E. J. F., 79, 83 Wood, F. P., 210, 246 Wood, J. D., 210, 212, 213, 240,247 Wood, L., 233, 249 Woodbridge, H., 16, 19, 20, 88 Woods Hole Oceanographic Institute, 79,100

Wooster, W. S., 257, 258, 263, 264, 278, 279, 284, 288, 289, 295, 296, 303, 311, 315, 333, 334 Wootton, V., 211, 227, 246 Wright, E. P., 340, 454, 456, 475, 508 Wyllie, J. G., 258, 272, 278, 316, 332 Wyrtki, K., 258, 261, 262, 271, 278, 284, 288, 290, 292, 293, 299, 316, 334

Y Yamada, M., 469, 508 Yoneda, T., 207, 221, 222, 253 Yonge, C. M., 40, 49, 54, 100, 345, 359, 363, 364, 365, 366, 368, 370, 372, 373, 374, 390, 402, 407, 431, 445, 476.. 508,. 509 Yoshida, K., 260, 262, 265, 278, 334

627

AUTHOR INDEX

Yoshimuda, J., 205, 253 Yoshimura, H., 112, 203 Young, E. G., 212, 253 Young, J. Z., 228, 252 Yudkin, W. H., 206, 209, 242

Z Zappacosta, S., 206, 209, 220, 227, 252 Zernov, S. A., 476, 509 Zilliow, E. J., 129, 204 Zobell, C. E., 441, 509 Zvorykin, N. P., 448, 449, 451, 509

This Page Intentionally Left Blank

Taxonomic Index A Abyeeascidia wyvillii, 71 A w t i a , 146, 160, 164, 162 c l a d , 131, 146, 148, 160, 162, 168, 171, 187, 189 toma, 129, 131, 163, 164, 169, 164, 187

ACMM f u l h , 446 Achnantea taeniata, 185 Aotinia, 206 Adagnesia: bi$da, 72 Agrnenellum q;uadmcplicatum, 112

Agneeicc depreesa, 72 glaoiataG, 68 Allomcarpa ilumccrtane, 66 Arnphidinizcrn carterm, 112 Amphitrite, 209 Amula orietatct, 49 Andira vemnifuga, 480 Anemonia, 206 Anodonta, 232 Anomalocera patersoni, 142 Anthopleura, 206 Aplidium abpwum, 71 wmtellatzcm, 32 fuegieme, 66 multiplicatzCm, 29,30 nordmccnni, 11, 17, 62 pallidum, 11, 37 p n c t u m , 11 retiforme, 68 zostericola, 37 Apomatue, 209

Arbaoia, 210 Arm, 207 umbonata

Ar c h i d k t m a aggrqatum, 29, 30 Architrophqja, 469 Arenicola, 209, 220, 224, 225, 226, 227, 235 aasimilia, 226 Oristata, 219, 220 m1zcb, 224, 225 Artem&, 129 8dhU, 129, 130, 142 As&&, 46, 49 &a, 4 callosa, 43, 64 wmhilega, 43 intwmpta, 6 , 22, 63 mentula, 17,26,36,40,43,46, 62,63 n+a, 6, 12, 21, 22, 27, 28, 48, 80 Bydneaenais, 6 virgin-, 43 Ascidbola rosea, 61 Ascidiella aepersa, 26, 33, 34, 36, 37,43, 44, 61, 52, 63, 80 embra, 36, 37, 40, 42, 43, 48 Astaous, 228, 236 Astarte borealia, 37, 40 AstePias, 210, 226, 227, 236 &em, 236 AsteriolEella japonica, 109, 120, 121, 123, 124 Astropecten, 2 10 aurantiacuS, 231 AwEouinia, 209, 213, 226, 231 Aurelie, 206 Auioula, 208

B B a o t r o n o p h , 338, 366, 362, 369, 376, 376, 379, 386 629

530

TAXONOMIC INDEX

Bactronophorua thwacitw, 339, 340, 342, 143, 346, 369, 386, 474

Bahnw amphitrite wmmunie, 464 balanoides, 141, 142 Bankia, 340, 345, 350, 355, 360, 361, 362, 369, 370, 371, 374, 375, 385, 390, 402, 404, 416, 417, 428, 442, 443, 453, 472 anechoercsis, 344, 347 auatrdia, 343, 344, 347, 369, 385, 426, 428 barthelowi, 344, 347 bipalmulata, 339, 342, 343, 347 bipennata, 339, 343, 344, 347, 429, 430 brevia, 344, 347 cumpanellata,339,340,341,342,343, 344, 347, 369, 386, 391, 396, 399, 406, 410, 411, 416, 427, 429, 430, 453, 457, 459 carinata, 339,340,341,342,343,344, 345, 347, 349, 362, 369, 372, 375, 380, 400, 402, 413, 416, 424, 426, 430, 460, 461 &ba, 344, 347 dwtructa, 344, 347 Jimbriatula, 344, 347, 467 foster;, 344, 347 gouldi, 344, 346, 347, 349, 366, 368, 365, 367, 369, 370, 376, 379, 380, 381, 382, 383, 384, 386, 386, 388, 390, 399, 401, 406, 415, 416, 426, 426, 429, 450, 451, 463, 460, 469 gracilb, 343, 344, 347 hwaiiercsis, 417, 463 indka, 345, 349, 355, 366, 368, 366, 368, 369, 370, 372, 373, 376, 376, 378, 379, 380, 382, 383, 384, 385, 386, 387, 388, 389, 391, 399, 400, 402, 403, 404, 406, 413, 414, 427, 442, 443, 460, 461 marten& 343, 344, 347, 429 minima, 364, 366, 368, 376, 448, 453 m r d i , 339, 340, 343, 344, 347 orcutti, 343, 344, 347 philippine&, 344, 347 rochi, 339, 340, 341, 342, 343, 347, 366

Bankia aetacea, 344, 347, 349, 369,370, 385, 391, 399, 406, 416, 416, 419, 426, 429, 441, 443, 446, 460, 463 zeteki, 344, 347, 479

Bankia (Bankiella) gouldi, 361 m i n i m , 345 Bankia (Nausitora) jam&, 360

Bankia (Nwbankia) barthelewi, 360 Bankiinae, 340 Bathymcidia vmculoaa, 72 Bathyonow, diaooideua, 73 herdmani, 73 minutua, 73 mirabilie, 73 Bathypera aplendena, 74 Bathyat yeloidea enderbyanua, 38, 74, 78 Benthuscidia michxmlaeni, 71 Boltenia echinata, 43, 64 ovqera, 64 vilio~a,21 Boltenwpak penenti, 46 Boatrichobranchua digonae, 34 pilularie, 34, 47 Botrylloides, 16, 31, 49 leachi, 17, 33, 43, 48, 49 nigrum, 12 Botryllua, 20, 31, 32, 49 planua, 12 achloaaeri, 6, 8, 9, 11, 16, 20, 29, 30, 33, 36, 43, 44, 47, 48, 49

Bouteria cumpechiana, 480 Boveria, 357, 469 teredinidi, 469 Brachiomonas, 134 szcbmrina, 134 Branchiodontw, 208 Brioreurn, 206, 227

TAXONOMIC INDEX

Bzcgzcla, 27 Bulla, 207 Bunodea, 206 Bunodosoma covernata, 221 Busycon, 207 perversum, 221

Chelyosoma, 26 columbknum, 27 incceqwcle, 71 macleayanum, 26, 27, 36 productum, 27 Chilostomatcc, 212 Chlamys, 40 septemradida, 40 Chondrua, 212 Chryaophyllum

C

c&nitO,480

Cachonina, 115 niei, 114, 115, 127 Calanua, 132, 133, 134, 146, 148, 149, 152, 154, 156, 157, 158, 159, 209

p n m a r c h h a , 130, 131, 132, 133, 136, 137, 138, 139, 140, 141, 142, 146, 147, 148, 150, 153, 155, 162, 163, 164, 165, 167, 168, helgolandicua, 130, 135, 141,142, 147, 149, 150, 155, 162, 163, 165, 167, 168, 171 hyperboreua, 135, 137, 140, 148, 150, 168, 170

144, 156, 170 145, 164, 149,

Callinectea sapidzcs, 48 Callionymus lyra, 142 Calyx, 206 Cancer, 210, 228, 240 pagurms, 228 Carcinides maenas, 152 Carcinua, 210, 228, 229, 230, 234, 235, 237 maenas, 228, 233 Camidaria, 207

Centropages humatua, 129

Ceranium, 2 12 Cetengraulis mysticetua, 277 Chaetoceros, 112 a s n e , 109 curvisetum, 109 decipiens, 109, 133 gracile, 120, 123, 124 Cheilostomata, 206 Chelura, 466 terebrana, 473

531

C i m , 3, 4, 21, 22, 25, 26, 40, 46, 80, 210

i n t e a t i d i s , 2, 3, 7, 8, 13, 17, 21, 23, 25,27,33, 34, 35,37,42,43,44,45, 80, 81, 82 irrteatinalis f. typica, 7, 24 Clavelina, 30 lepadgomis, 11, 17, 43 oblonga, 33 pi&, 33 Clibanariua, 210 vittatua, 221 Clymene, 209 lumbricoides, 224 Cnemidocarpa, 73 bgurcata, 73 bythia, 73 d i g o w , 73 drygalskii, 73 nordenakjoldi, 77

Coccolithua huxleyi, 120, 125 Cordia alwdora, 480 Corelh eumyota, 67, 68 parallelogramma, 13, 26, 43, 51, 62 Willmeriana, 20, 26, 46, 50 Corellopsis tranalwida, 71 Corollospora plchella, 458 Corynaclis, 206 Corynascidk, 76, 77 herdrnani, 77 sedens, 000, auhmi, 71, 77 Coscinodiscua, 112, 277

oentralia, vm. paci$ca, 109

632

TAXONOMIU INDEX

~08cinodie~ua li?leatua, 118,120 waileaii, 120 Crangon, 210 CrCl8808trea, 208, 233, 464 vwginim, 221, 240, 449, 469 Crepidulcc, 207 Crkosphera, 134 cartercce, 112 elongata, 133 Cryptochiton atelleri, 436 Cryptomonas, 133 Crypto& @l&na, 463 Culwlua, 6, 39, 77, 78 antarctkua, 74 invereue, 74 moeeteyi, 74 muwayi, 74, 77 p a m y 76 perluoidua, 74 pyramidal&, 74 recumbem, 74 ahmi, 74 u a c h k o d , 76 willemo&, 76 Cyanea capillda, 168 Cycloporw, papilloma, 49 cyclotellcc myptim, 128 mna, 6, 120, 124 Cylindrotheca clo8terium, 124 cb8tePium vm. Califmica, 116 cy8todytee dellechiajei, 17

D Daorydium franklinii, 480 Ddergia retuaa, 480 Deleaaeria 8a;ngUirCea, 37 Dendrodoa groseularia, 10, 11, 17, 26, 42, 43, 46, 49

Deeidicus, 208 Deamareetia, 212 Dextiocarpa 80&kWk, 17 Diazona, 30, 42 dolacea, 17, 30, 33 DicaPpa

p c i f i c a , 38, 73 eimplex, 73 Dicyathifer, 338, 362, 369, 376, 376, 386 manni, 339, 340, 341, 342, 343, 346, 369, 385 Didemnm mndidum, 11, 29 candidurn lutariurn, 12 conchyliaturn, 80 helgolandicurn, 17 Studeri, 67 Diplosoma, 16, 36 cupzcliferum, 16 lkterknum, 11, 17, 21, 33, 37, 49, 80, 81 macdolucldi, 12 singulccre, 37 drena, 64, 66 DietaplicC, 16 cylindrica, 3, 16 durbaltenai.9, 16 galathem, 71 ro8ea, 17 unigemnia, 61 Ditylum, 134, 164 brighwelli, 116, 117, 120, 125, 127, 164 Donux, 208 D ~ O p S 207 ~ , Doropygua, 61 Doeinicc, 208 Dudiella Balina, 112 tertiolecta, 117, 120, 121, 123, 126, 126, 128

E EoteinascidicC turbinata, 43

Eledone, 208

633

TAXONOMIO INDEX

Ftk&?&.h

EdWPh hunhnani, 64 Entermorpha, 80, 212, 239 EnteropG aphim, 61 Erado voluta, 48, 49 Eriocheir, 210, 228, 233, 236, 236, 237 Euoalyptua marginata, 479 Edktoma, 66 digitaturn, 16, 16, 18 fantwknum, 16, 17, 18 illoturn, 17 ritteri, 16, 21 w t u r n , 16 v&eum, 71 Eugymnanthea, 469, 470 cornmenaalis, 471 Eugyra cwrnbaeckcte, 3, 38, 39 arenoaa, 34 Euherdmak, 16 c l a @ f m i a , 14, 17, 21 Eupera chuni, 76 Euphauk paoifica, 129, 147, 148, 160, 168 auperba, 143 tiacantha, 131

wegmneis, 49

G kterascidh, 6 aanderei, 6, 76 Gelidiurn, 212 Geodia, 206 gigas, 227 Gigartina, 212 Glycera, 209, 213, 231 Gkmonia b t l % h O S h & , 468 Gonyahx afrkana, 109 cochlea, 109 polyedra, 116, 120

~oora/iodonia wtanm, 49 modoswr, 49

Gonophyam gullrnwenai8, 61, 62 Grafilla brami, 471 Chyph, 208, 236, 236 Gyrnrwdinium aplendem, 120

Ewylepla l e o p o b , 60

H

Euaideroxylon zwageri, 480 Euterpina acutifrorw, 129 Eutima, 471 Evadne apiniifera, 168 Emviella, 112

H&W&,

206

Halwth, 207 HaloCynthia aurantium, 49 papdha, 40,41 roretzi, 81 H&ptiiU% long~comk,171 Hd08plKWiU

F Faaciolaria, 207 distana, 221 Ficulina, 206 Fungulw antarcticw, 74 cinereua, 74 Furcellaria, 212

q d r k o r n u a t a , 458 Ha&&& BiliQuoBcb, 37 Helix aapera, 446 nernordia, 446 pomath, 446 Hemistyela pilosa, 74

534

TAXONOMICY INDEX

Herdmania mmus, 53

Heterostigma f q e i , 38 s e p r , 39 singulare, 75 Hexacrobylua, 5 a r c t h , 77 indicua, 75, 77, 78 psammatodes, 75,77, 78 H o m m , 210, 229, 234, 240 vulgaris, 228 Hydrobia, 207 Hymenimidon. 206, 226 camneula, 226 Hypobythiua calywdea, 72 Hypsktozoa, 30 f m e r i a n a , 14, 16, 17, 18, 32, 33 obscura, 71

I Idalia elegana, 49 Isochryaia galbana, 120, 123

K Katherinct, 437 tunicata, 436 Kuekenthalia borealis, 74 Kuphus, 338, 356, 357, 362, 369, 385,

Limax

cinereoniger, 445 Limnoka, 210, 417, 459, 466, 467 lignomm, 473 L&mulua, 210, 240 Lissoclinum argyllense, 11 patella, 54 p l v i n u m , 54 Lithophaga, 208 bisdoatcc, 221 Littorina, 207 Loligo, 208,228 forb&, 228 Loliguncula, 209 brevis, 221 h i d i a , 210 ehthrata, 221 Lulworthia, 458

LudricUS, 231 Lyoaetis senegalemis, 472 Lyrodua, 340, 362, 369, 370, 375, 390, 401, 429

389,444

polythalarnia, 344, 346, 369, 385

.L Lagenophrys, 469 Lamellaria perapicua, 49 Laminaria ochroleuca, 35 Latideria borealis, 109, 164 Lander, 235, 236 serratus, 234 8qu&&, 234 L e i o h , 209

Lernbos intermediua, 154 Leptoclinidea faeroenais, 71 Leptocylindw danicua, 120 Leptomysis linpura, 143 Leucothoii spinimpa, 53 L i g i a , 210

a@&, 339, 342, 343, 347, 401 bipartita, 344, 346, 415, 425, 426 dkgensiS, 401, 406 mwsa, 339, 342, 343, 344, 346, 363, 369, 385, 401

mediolobatcc, 344, 347, 369, 385, 401 pedicellatus, 339, 342, 343, 344, 347, 360, 361, 365, 368, 369, 381, 385, 396, 401, 404, 406, 443 takanoshhen&, 344, 347, 369, 385

fl Macrocystis, 212 M&a, 208

535

TAXONOMIO INDEX

Ma&, 210, 229 equinado, 228 Mangqera indica, 427 Manilkara dariensis, 480 Marteaia, 367, 411, 417 jragilb, 436 striata, 388, 410, 419, 436, 438, 457 Megalodicopia hiam, 72 Meganyctiphnea nowe@, 130, 143, 144 Meloeira, 277 Mereenaria mereenaria, 367 Metandrocarpa taylol-i, 15, 16, 30 Metridia, 139 longa, 143 Metridium, 206 Microcosmus, 40, 41, 46, 63 claudicuns, 62 kura, 80 mult~ntaculatua,54 eabatieri, 40, 41, 42, 45, 54 8uldua, 4, 36, 40, 41, 42, 45, 81, 82 vulgarb, 35, 41, 42, 46

Mimatyela clauata, 73, 76, 77 Mitella, 209 Mitrella lunata, 49 Mnemiopsb, 471 Modwlus, 464 Molgula, 3, 4, 76 bathybia, 75 citrina, 16, 17, 20, 43 galathem, 75 mnhattenab, 13, 26, 27, 35, 40, 42, 43, 44, 46, 48

occulta, 46 eluderi, 67 verrilli, 75 Molgula (Molguloidea) aphmroidea, 75 Monochrysk lutheri, 112, 120, 121, 123 Murex, 207

Mmculus mamoratm, 53 Mya, 222, 239, 240 arenaria, 40, 367 Mytilus, 207, 211, 221, 222, 228, 229, 232, 233, 235, 236, 445, 462

edulk, 215, 222, 232, 236 Myxicola, 209

N Naasarius obsoletua, 142 Nausitora, 340,355, 356,361,362,369, 371, 375, 376, 385, 428, 454, 456

brazilknsis, 454 dryaa, 344, 347, 428, 454 dunlopei, 339,340,342,343,347,369, 370, 381, 385, 389, 401, 428, 454, 456 exwlpa, 344, 347, 428, 454 jluviatilia, 454 juaticula, 347,364,365,369,370,381, 385, 389, 428, 454 hedleyi, 339, 340, 341, 342, 343, 345, 347, 355, 356, 357, 358, 359, 365, 368, 369, 370, 373, 374, 376, 377, 378, 379, 380, 381, 383, 384, 385, 386, 387, 388, 389, 390, 391, 392, 393, 394, 395, 397, 398, 399, 401, 410, 411, 412, 413, 415, 418, 419, 420, 421, 422, 423, 427, 428, 431, 432, 433, 435, 436, 437, 438, 439, 454, 455, 456, 469, 470, 482 lamwlata, 454 Oahumaia, 454 NmMhea, 209

Neotandra rodioei, 479 Nwdeleea, 2 12 Nwmysk integer, 143, 148, 150, 152 rayii, 147, 150 Neopanope, 210 Neoteredo, 338, 356, 362, 369, 371, 375, 376, 379, 385

reynei, 343, 344, 346, 369, 381, 385 Nephrope, 234 Neptunus, 210

536

TAXONOMIU INDEX

N~reilepa~~ fuoata, 472 Nereia, 209, 213, 231, 235, 472 Nerine, 209 Nitzschia atlantica, 109 closterium, 109 closterium forma minutissima, 117 pungem, 109 Noetia, 208 Notodelphys allmani, 51 Nototeredo, 340, 360, 362, 364, 369, 374 edax, 339, 342, 343, 347, 369, 370, 375, 385

knoxi, 344, 347, 364, 369, 375, 385 norvagica, 344, 347, 348, 355, 356, 360, 363, 364, 369, 371, 375, 385, 401, 402, 424, 425, 468

0 Octacnemus, 5 bythius, 72 herdmani, 72 Octopus, 208, 229 Oithom, 154, 187 sirnilis, 150, 153, 154 Oligotrema, 75 paammitee, 75, 77 Oliva sayana, 221 Olhia, 207 Ommmtrephes, 208 Opque, 212 Orchistoidea, 210 Ostrea, 208, 236, 445

P Pachygrapsus Pachymatisma, 206 Pagurus, 210 pollicaris, 221 Palaemon, 210, 234 Ekga?LS, 234 serratus, 234

Palinurua, 229 vulgaris, 228 P a n u l k s , 210 Paramolgula gregaria, 4, 66 Patella, 207 Pecten, 208, 211, 229 Pectunculus, 207 PdOTWh corrugata, 8, 11, 18, 34 Penaeus, 210 azecus, 221 Penilia avirostris, 168 Peridinium trochoideum, 109, 149 Perinereis, 235 Perophora, 30 bermudensis, 33 listeri, 17 viridia, 16, 20, 21, 29 Phaeocystia, 115 Phaeodactylum tricornutum, 112, 117, 121, 123 Phalluaia mammillata, 4, 52, 82 Pharyngodictyon mirabik, 71 Phaecolosoma, 206, 227 elongatum, 224 moduli&rum, 225 Phoronopsis harmeri, 231 Physalia, 206 P&ZStt?r,210 Pinna, 207 Pinnotheres, 53 Platyodon, 365 Pleurobrachia pileus, 141, 142 Pleurobranchua membrameus, 49 Pleuroncodes planipes, 274 Podoclavella, 7 1 Podon polyphemoides, 168

537

TAXONOMIU INDEX

Polinicea, 207 duplicata, 221 Polycarpa, 63 albatrossi, 73 delta, 38 fiboea, 34 p m m ' a , 40, 41, 49, 81 pseudo albatrossi, 73 tinctor, 14, 18 Polyeitor cires, 18 crystallinus, 17 fungqormis, 7 1 mutabilk, 28, 29 Polyclinum aurantium, 11, 17, 36, 42, 62 Polysiphonia, 212, 239 Polysyncraton laoazei, 35 naagnilarvurn, 16, 17 Polyzoa opuntia, 66 reticzclata, 67 Pomatoceros, 209 Pontonia, 52, 53 jlamomaculata, 52, 63 Pwphyra, 212 Potamon nilotkus, 235 Potmnopyrgus ciliatua, 412 Prorocentrum scutellum, 109 Protoholozoa pedunculata, 7 1 Protula, 209 Psammostyela delamwei, 39 Pseudocalanus, 142, 164 nainutus, 129, 150, 153, 154 Pseudoceros crozieri, 50 Pseudodistoma arboreaiena, 17 Ptilota, 2 12 Psiloteredo, 338, 362, 369, 370, 375, 385 amboineneis, 368, 370 healdi, 344, 346, 369, 466 megotma, 344, 346, 349, 365, 363, 369, 396

Psiloteredo senegalensis, 344, 346, 369 Pycnoclavella, 16 stanleyi, 16, 17, 21 Pyura, 12, 33, 63 bwvetenais, 39 chathamen&, 68 chilensis, 33, 35, 48, 81 gewgiana, 39 legumen, 39, 66 microcosmus, 17 pachydernaatina, 68 praeputialk, 33, 50 spinosiseima, 68 stolonifera, 33 tesselata, 62

R Ran&, 208, 222, 232 cuneata, 222, 232 Renilla, 206 Rhimhnua naeutus,129, 163, 164, 171 Rhizomolgula globdark, 34 Rhizosolenia robzcsta, 119, 120 stolterfothii, 120 Rhizostow, 206

S Sabellaria, 209 alveolata, 224 Sagartia, 206 Sagitta elegana, 142, 165, 168 hispidia, 148, 150, 155, 162 Sepia, 208,229 oflcimlis, 228 Septifer, 207, 220 S e r p h , 209 Sidnyum turbinatum, 11 Siphonaria, 207 lineolata, 221 zelandh, 239 Sipumulus, 206

538

TAXONOMIU INDEX

Skeletonema, 134, 136, 149, 169, 160 costalum, 109, 112, 120, 126,126, 133, 185, 186

Spathoteredo, 340, 361, 362, 370, 376, 385

obtusa, 342, 343, 347, 369, 386 a p t h a , 344, 347, 369, 386 S p h r o m a , 466 Spirontocaris, 210 Spondylua, 208 Strongylocentrotus, 2 10 droebachienaie, 238 Styela, 73 bathybia, 72 olava, 36, 81 c o r k e a , 6, 26, 37, 40, 43, 46, 49 loculosa, 72, 76, 77 milleri, 72 nordenskjoldi, 73 paessleri, 66 partita, 17 plicata, 27, 44, 81 pusilla, 72 ruatica, 10, 43 sericata, 72 squamosa, 72 Stylochoplana, 472 Swartziawe panamensis, 480 Sywzoa, 15, 30 arboreacena, 68 s@illinoidea, 12, 17, 30, 31 Symplegma &ride, 12

Syncarpia l a d f o l i a , 479, 480 Syndiazona, 30 Synechococoue, 128 synoicum adareanum, 16 argua, 29 georgianum, 17 tentactdatum, 71 Syracosphaera, 134 carterae, 112 elongata, 133

T Tabebuia gwzyacan, 480

Taenioplana teredini, 471 Talorche.at&z tricornuata, 474 Tectona grandis, 480 Tegula, 207, 233 Tellina, 239 Temora longkornk, 129, 134, 150, 163 Terebratella, 206, 2 12 Teredinidae, 399 Teredicola typica, 471, 472 Teredo, 208, 340, 345, 363, 362, 366, 368, 386, 410, 441, 467,

369, 370, 371, 374, 376, 376, 386, 388, 390, 391, 404, 406, 411, 417, 426, 429, 434, 440, 443, 444, 445, 449, 460, 466, 469, 471, 472, 474, 479, 480 aegypos, 344, 346 bartachi, 343, 344, 346, 368,401,406, 407, 429, 431, 464 clappi, 339, 340, 342, 343, 346, 362, 369, 386, 401, 429 diegensis, 391, 406, 453, 454 dilatata, 381, 382, 384, 388, 396,416, 474 fatalis, 402 fulleri, 339, 342, 343, 346, 362, 369, 386 furcifera, 339,340,341,342,343,345, 346, 349, 368, 369, 373, 377, 379, 381, 383, 384, 385, 386, 387, 390, 396, 401, 406, 407, 410, 412, 413, 416, 416, 429, 444, 460, 467, 468, 459, 469, 482 fwrcillatus, 410, 427, 460, 467, 469 gregoreyi, 427 healdi, 480 japonica, 415 johmoni, 343, 344, 346 manni, 368 megotara, 349,357,368,363,368,376, 380, 416, 449, 460, 474 milleri, 417, 427, 464, 472 mindanemia, 343, 344, 346 miraJOra, 479 morsei, 396

639

TAXONOMIO INDEX

Teredo

Teredothyra, 338, 362, 363, 369, 376,

mdia, 342, 343, 346, 346, 349, 353, 364, 366, 370, 391, 406, 444, 469,

366, 367, 368, 360, 363, 367, 368, 369, 374, 376, 381, 384, 386, 388, 389, 394, 396, 401, 402, 403, 416, 416, 426, 429, 441, 448, 449, 460, 461, 453, 469 norvegica, 348, 366, 368, 363, 369, 376, 380, 384, 390, 404, 416, 416, 419, 424, 441, 448, park&, 396, 401 pediCdl&, 364, 366, 384, 403, 406, 409, 423, 424, 426, 436, 448, 460, 464, 467, 469 pedkellatue, 349 pEi%ti,412 philippi, 440 poculger, 344, 347, 369, 385, 420, 464 prtoriceneia, 344,347 reyne, 479 .ise.foo.i, 364, 366 eomerai, 343, 344, 347,401, 429 trimgularie, 339, 343, 344, 347 tmll~ormia,362, 417, 464 utrioulus, 364, 366, 424, 448

364, 378, 390, 404, 443, 466, 368, 407, 449 406, 438,

401,

Teredo (Lyrodua) mediolobata, 396 pedkllata, 431 Teredo (Pailoteredo) pet&%, 362 senegalensis, 362 Teredo (Teredo) beaufiwtana, 369 Teredo (Teredothyra) dv?ninke&, 364 Teredophilua renhla, 472 Teredora, 338, 362, 361, 362, 364, 369, 370, 371, 374, 376, 376, 381, 386, 444 gregoreyi, 373 d l e o l u e , 344, 346, 362, 366, 369 prheeaae, 339, 340, 341, 342, 343, 345, 346, 368, 369, 310, 311, 373, 376, 377, 379, 381, 384, 386, 386, 387, 389, 390, 482 A.H.B.--O

376, 386

atwoodi, 426 dominioeneia, 344, 346, 364, 369, 401 exmvata, 339, 344, 346 maloootana, 342, 343, 346, 360, 389, 401, 426

amithi, 330, 342, 343, 346, 425 Tetraaelmia maoulata, 112

Thake, 207 ?tmmastoma, 221 Thdaa&nema, 277 ndzachwidea, 109 TMaaabaira, 140, 163, 164, 166 ckc@k?la, 109 .fluviaMia, 128, 120, 136, 164 nordemk&%dii, 109 Thetk, 206, 226 lyncuriurn, 226 Thyone, 210, 221

Thyaamiieecc inermia, 143 TG?* d i f o r n h , 129 Torpdoapora radhkz, 468

Tortanua dkcauddue, 129

Travbia, 224 Triohodecrmium, 103, 182 Trichotropis mncellata, 40 Tpidaea, 212

Tr&didemnum, 64 cyclop, 64 deleaaeriae, 37 niveum, 36 &ride, 64 Trochilwidea, 469 Tubulamcl * ,27 Turbo, 207 Tylobranchwn apeoiofrum, 17

U Ulva, 212, 230 Uperotua, 338, 362, 369, 370, 311, 376, 376, 381, 386, 444 16

540

TbXONOMXl INDEX

X

Uperotua

clrcvue, 339, 341, 342, 343, 346, 369, 424 lieberkindi, 344, 346 pamme&, 344, 346 rehderi, 339, 341, 343, 344, 346, 369

Urtxhis

x~.!OSpOng~, 206 Xylophqa, 370, 376, 380 dorsalis, 367, 386 Xylotrya J i m b r b , 460

m p o , 231

V Veluth uelutim, 49 Venw, 208 VoVoleella, 208

Z Zirphaea, 367 criapatu, 366, 367 Zootbmnium, 469 Zoetera, 37, 40

Subject Index A Acanthocephalans, 472 Adesmaoea, 366, 366, 367, 370, 371, 386

Adriatic, 448, 463, 454, 471 Africa east coast, 342, 343, 346, 347, 430 west coast, 346, 347, 472 Agadir, 286 Agnesiidae, 66, 71 Agulus Current, 289, 298 Al Walat, 279 Alaska, 274 Alaska gyral, 268, 296 Alaskan peninsula, 63 Albatroas Philippine Expedition, 424 Algae, 37, 64, 55, 80, 129, 132, 136,266, 267, 270, 271, 277, 286, 289, 302, 303, 304, 306, 311, 317, 318, 407, 429, 463 blue-green, 103, 128 calcareous, 37

green, 65 large brown, 36, 37 reproductive rate, 267 symbiotic, 64 t a k e in, 212, 239 Unicellular, 129, 407 Algal cells, 4 Algoa Bay, 68 Alpheids, 53 Ambrizette, Congo, 426 Amino acids concentration in marine invertebrate nerves, 229 concentration in marine invertebrate tissues, 221, 231, 232, 233, 234, 236, 236, 237, 238, 241

distribution in marine invertebrate nerves, 228 in crustaceans, 230, 233 in lobsters, 213, 214 in molluscan nerves, 230 Amphibia, 227

Amphipods, 61, 52, 162, 474 &B commensals in ascidians, 62 gammarid, 164 nitrogenexcretion, 162 Anchovy, 273, 274, 276, 277, 286, 309, 314, 316, 316,318, 324

distribution, 316, 317 Peruvian, 309, 316, 316 spawning, 317 Andaman Islands, 257, 290, 298, 299, 300, 339

Andaman Sea, 290, 308 Andhra coast, 339, 340 Angola, 287, 293, 320 Angola Dorre, 293 Annapolis, Maryland, 463 Annelids seasile, 80 taurine, in, 209, 211, 239 Antarctic, 56,67, 64,66, 68,69,70,129, 131, 182, 266, 267

convergence, 66 Drake Passage, 183 Anti-boreal, 65, 66, 68 convergence, 66, 67, 68 South American, 66 (Subantarctic)islands, 67 Antipodes, 267 Antofagasta, 278, 284 “Anton Bruun” expedition, 289, 294. 296

Apalachicola river, Florida, 467 Arabian Sea, 181, 268, 288, 296, 296, 299, 418

&afwa Sea, 290, 298, 300 Archinotodelphyidae, 62 Arctic, 65, 67, 63, 64, 65, 70, 183 Canadian, 183, 184 Ardrossan, Scotland, 26 &ice, 278, 284, 296, 318 Aristophanes, 336 Arrow worms, 306 Arthropods ta;urine, in, 211 Asamushi, Japan, 12 641

642

SUBJECT INDEX

Ascidians abundance, 34 abundance factors, 36-47 abyssal, 5, 77, 79 abyssal species, 69 adaption, 36, 37, 38, 39, 40, 41, 42, 43

as diet of predators, 48, 49, 50 aa protective cover of timber against wood-borer attack, 461,462-465 as source of chemicals, 82 asexual reproduction, 6, 22, 29, 30, 32

at depths greater than 2000 m, 70-79 atrial cavity, 14 attachment to supports, 36-42 biology of, 1 et e q . biomass, 33-35 boreo-arctic species, 8, 11 branchial sac, 2, 4, 5, 50, 51, 52, 53, 81

breeding, 6-22, 29, 30 breeding on Scottish west coast, 11 breeding season, 6-13 brood pouch, 14, 15 budding, 29, 30 changes in populations, 35-36 colonies, 15, 20,27,28,29, 30, 31, 36, 49, 51

commensals, 47, 50-55 culture, 81 deep-water, 5, 69-79 deposit-feeders,5 distribution factors, 36-47 ecology, 33-47 economic importance, 79-82 endemic of American Atlantic, 60 endemic of American Pacific, 61 endemic of Antarctic, 64, 65 endemic of A n t i b o d regions, 65, 66, 67

endemio of Arctic, 63, 64 endemic of Australia, 59 endemic of boreal American Atlantic, 62. 63

endemic of boreal European Atlantic, 61, 62

endemic of Indo-Malaya endemic of Japan, 68 endemic of Mediterranean, 60, 61

Ascidians-continued endemic of New Zealand, 67, 68 endemic of north-eastern Pacific, 63 endemic of north-western Pacific, 63 endemic of Red Sea, 59 endemic of South Africa, 68 endemic of West Africa, 59, 60 endemic of Western Indian Ocean, 58, 59

endostyle, 2, 3 epibionts, 40, 41 faunistic relationship, 55, 56, 58 feeding, 2-6 feeding mechanism, 2-4 filter-feeding, 3, 4, 5, 50, 81 fission of colonies, 6 food, 4-6 food of commercial fish, 81 food of man. 81-82 fouling, 79-81 fusion of species, 31 gametes, 6, 13, 14, 15 geographical distribution, 55-79 gonads, 6, 11, 13, 14, 30, 77 growth, 22-33, 35 interstitial, 6, 39 larva, 6, 7, 10, 11, 12, 14-22, 30, 43, 45, 46, 55, 81

life cycle, 22-33 mortality, 7, 22-33, 35 mud-dwelling, 47 mutualism, 50 neural complex, 14 neurosecretory cells, 14 numbers, 33-35 oesophagus, 51 oral siphon, 3, 5, 6, 48, 50 oral tentacles, 3, 5 oviduct, 14, 15 parasites, 47, 50-55 phoresis, 50 photophilic, 41 population density, 35, 36 predators, 47, 48-50 rhizoids, 36 salinity tolerance, 42-43 sand-dwelling, 39, 47 senescence, 27 sexual reproduction, 6, 8, 14, 29, 30, 32

643

SUBIJECT INDEX

Ascidiens-wntkd shallow-water, 5, 56-69 size-distribution, 7, 8 south boreal species, 11 spawning, 13-14 stabilization of a m bed, 47 stalked rock-dwelling forms, 39 stigmata, 2 sub-populations,47 succession of generations, 22-33 sudden mortality, 27 symbionts, 47, 50-55 tadpole, 15, 16, 22 temperature tolerance, 44 test filaments, 37 thorax, 14, 15 turbidity effects, 44, 45 uptake of harmful substances, 82 world distribution, 65, 57 zoogeography, 55, 57, 70, 79 Ascidians, abundance factors biotic, 46-47 light, 45 salinity, 42-43 substratum, 36-42 temperature, 44 turbidity, 4 4 4 5 Ascidians, distribution factors biotic, 45-47 light, 45 salinity, 42-43 substratum, 36-42 temperature, 44 turbidity, 44-46 Ascidians, as fouling organisms assessment, 79, 80 on oyster beds, 81 on buoys, 79 on hulls of ships, 79, 80, 81 on fixed harbour installations, 79 Ascidians, larva adhesive papillae, 16 anterior ampullae, 16 behaviour, 19-20 development and relectse, 1P.16 epidermal vesicles, 16 evolution, 22 fixation to substratum, 20, 21 geographical distribution, 55-79 gregarious settlement, 45, 46

Ascidiam, l a r v w n t i n d influence of light on, 45 influence of salinity on, 43 influence of temperature on, 44 life span, 19, 20 metamorphosis, 20, 21 oceanic transport, 55 papillae, 16, 21 pelagic life, 56, 81 settlement, 20-22 size, 18,19 structure, 16-19 swimming speed, 18 types, 17, 18 Ascidicolidae, 52 Ascidiidae, 16, 37, 39, 72 Ascomycetes, 458 Asterubin, 210, 224, 226 Atlantic, 56, 60, 61, 63, 64, 69, 70, 77, I

103, 116, 256, 266, 294, 302, 320, 344, 464,466 American, 56, 57, 60, boreal American, 62, born1 European, 61

257, 260, 293, 428, 429, 448, 61, 415 63

“Atlantide” Expedition, 60 Atlantique sud Expedition, 425 Auckland Island, 67 Auckland, New Zealand, 12,80 Australian waters, 57,69,257,268,288, 290, 296, 298, 299, 300, 301, 308, 319, 342, 343, 346, 347, 430, 472, 475, 480, 481, 482

B Bacteria, 4, 5, 102, 103, 106, 130, 146, 147, 192, 223, 371, 442, 443, 444, 446, 446,458 denitrifying, 103 taurine in, 212, 223 Baia dos Tigros, 279 Baja California, 269, 271, 272, 273, 278, 281, 296, 318, 319 Balanids, 474 Baltic Sea, 37, 40, 43, 62 Baluchistan, 289 Banda Sea, 290,298,300,319,424 Bankiirm, 360

544

SUBJECT INDEX

Banyuls-sur-Mer, France, 40, 41, 42, 44, 46, 64 Barnacles, 80, 463, 464 Barnegat Bay, 406, 416, 471 Bathylagidae, 274 Bay of Aabenraa, Denmark, 481 Bay of Bengal, 266, 290, 298, 299 Bay of Biscay, 62 Beaufort, 406, 416, 417, 419, 460, 463, 469, 460 Bellingshausen Sea, 64 Benguela Current, 68, 266, 266, 267, 279, 284, 286, 287, 288, 296, 300, 302, 306, 308, 309, 311, 316, 318, 319 Benthic organisms, 161 Benthos, 34 sessile, 34 Bergen, 401 Berlin, 401 Bermuda, 116, 129,144, 148, 160, 162, 174, 178, 180, 181 Beypore river, 410 Biocoenoses, 42 Biscayne Bay, 168, 434 Bivalves, 40, 344, 346, 360, 363, 366, 367, 366, 366, 371, 380, 390, 407, 443, 444, 446 taurine in, 222, 232, 239 Black Sea, 42,143,168,396,449 Blastozooids, 16, 29 “Blois B MicTooomua”, 40, 46 Bohusliin, Sweden, 36 Bombay, 290,339,341,396,468 Boobies, 316 Boreal, 66, 62 Bothidae, 274 Botryllids, 28, 30 Botryllinae, 16, 37 Bottom deposits, 6, 6 Boveridae, 469 Branchiopoda taurine in, 206, 211, 212 Brazie, 464 Brazos River, Texas, 466 Brine shrimps, 142 Brisbane river, 464, 466 British coats, 26,449,460,479 British Columbia, 63, 272, 274, 316, 406,416,419,426, 460,463,477

Brittany, France, 39, 47 Bryozoa, 41, 80, 429 taurine in, 212 Burma, 290,298,299,342,343,416 Buzzards Bay, U.S.A., 34

C Cab0 Blanco, 316 Cab0 Frio, Brazil, 264 Calcichordata, 22 Calcofi programme, 281 Calcutta, 290, 340, 460 California, 61, 63, 80, 104, 106, 126, 266, 269, 273, 277, 280, 281, 282, 283, 291, 299, 304, 308, 316, 319, 322, 324, 326, 463, 464 California Countercurrent, 272 California Current, 267, 266, 269, 272, 274, 276, 277, 278, 284, 291, 296, 300, 304, 309, 311, 312, 316, 318, 319, 320 California Extension, 267, 322 Calloa, 284 Canaries, 278, 286, 296 Canaxy Current, 267, 278, 284, 286, 286, 287, 293, 294, 296, 299, 300, 302,306,309,311,318,319,320 Cap Blanc, 278,286,296,300,302,316, 318 Cap des Palmes, 288 Cap Frio, 287 Cap Ghir, 286 Cap Jubi, 286 Cap Timius, 286,287 Cap Vergas, 287 Cape Blanco, 272, 273, 278 Cape Cmanza, 278, 284 Cape Cod, 63, 137, 138 Cape Cunene, 286 Cape Flattery, 272, 278 Cape Gardafui, 268, 279, 289 Cape Hatteras, 62 Cape Mendocino, 272, 273,278,281 Cape of Good Hope, 266,279,319 Georges Bank, 137 Cape Point, 68 Cape Rein@, 294 Cape San Lucas, 273, 274, 316 Cape St. Vincent, 278

SWJEOT INDEX

Cape Thompson, Alaska, 33,63 Cape Vergas, 285 Carangidae, 274 N(L-Carboxyethyl)taurine, 2 12 Cariaco Trench, 293 Caribbean, 116, 344, 346, 347,481 “Carbo-Teredo” process, 476 Casablanca, 285 Catamarans, 468 Cattai Creek, 464 Cedros Islands, 273 Central America, 276 West coast, 346, 347 Ceylon, 290, 298, 299, 300, 319 Chaetognaths, 129, 141, 142, 144, 148, 166 Chatham Islands, 67, 68 Chatham Rise, 67 Chesapeake Bay, 416, 461 Chichester Harbour, England, 80 Chile, 300 Chincoteaugue Bay, U.S.A., 32 Chitons, 436, 437, 438 Chlorophyll, 114, 116, 166, 167, 168, 178, 179, 180, 181, 182, 183, 187, 188, 277 ChulalongkornLock,Rangsit Canal,466 Ciliates, 469 Reterotrichous, 469

cwna iMeatidi8 annual cycle, 26 aa fouling organisms, 80 body length, 23 breeding season, 7, 8, 13 effectsof environmentaltemperature, 23, 24, 26 feeding mechanism, 2, 3 filtration rate, 46 fixation, 21 growth, 23, 24, 26, 26 life cycle, 26 mortality, 27 population density, 36 salinity tolerance, 42 spawning, 13 uptake of radioactive materials, 82 Cionidae, 16 Cirripedes, 184 Cladocerans, 143 Clams, 469

545

Clavelinidae, 15, 16, 71 Clupeidae, 274, 306 Clyde sea-area, 137, 141, 142, 144, 160, 166, 166, 167, 162, 163, 168, 170 Cnidarians, 129 taurine in, 206, 211 Coasts of India, 339 east, 340, 341, 416 south-west, 339,341,416,419 west, 340, 341, 416, 447 Cochin, 289, 341, 394, 410, 411, 412, 413, 418, 419, 422, 423, 431, 466, 468 Cod, 48, 266, 276 Coelenterates taurine in, 212, 220 Columbia River, 272 Columbus, 336 Comer river, 340, 466 Commensal bacteria, 441, 442 Commensalism, 60-66 Congo, 291, 320, 481 Congo-Brazzaville, 288 Cook, 336 Copepods, 6, 61, 62, 64, 129, 130, 139, 141, 142, 148, 163, 164, 184, 301, 303, 304,306, 306, 317,471 as commensals in ascidians, 60, 61, 62, 63, 64, 66 aa commensals in molluscs, 472 aa parasites of shipworms, 471, 472 as parasites in ascidians, 60, 61, 62, 63, 64, 66 carnivorous, 306 diet, 134 egg production, 170 filtering rate, 139 nitrogen content, 141, 142, 143, 144 notodelphyid, 50 phosphorus content, 141, 142, 143, 144 rate of growth, 164, 170, 171 Corellidae, 16, 39, 66, 71 Coriolis force, 268 Cormorants, 316 Corsica, 42 Costa Rica, 268, 292 Costa Rica Coastal Current, 292 Costa Rica dome, 111, 260, 271, 292, 293, 300, 306, 308

546

SDBJEUT INDEX

Cotonou, 288 Crabs, 48, 61, 152 blue, 48 freshwater, 235 nitrogen excretion, 152 pea, 53 pelagic, 274 pinnotherid, 51 Creosoted timber, 466, 477 Cromwell Current, 262 Cromwell Undercurrent, 262, 263, 291, 296 Crustacea, 50, 52, 53, 142, 230, 233, 234, 305,419,468,460,462,466 entry into creosoted timber, 466 in destruction of shipworms, 467 in association with shipworms, 466, 467-474 mode of attack ‘ofwood, 466, 467 taurine in, 209,210,212,224,233 Ctenophores, 129, 306 in association with shipworms, 471 Cuba, 294, 417 Cuttlefish taurine in, 211, 228 Cypraeacea, 49 Cysteine, 217, 218, 219, 220, 221, 222, 223, 232 D-Cysteinolic acid, 212, 239

D Dakar, 278, 285, 286, 287, 288, 291, 293, 302, 318 Dampier, 336, 475 Davidson Current, 272 Decapods, 53 as commensals in ascidians, 62 “poikilosmotic,” 233 taurine in, 233 Deep scattering layer, 256, 307, 323 Deep water, 265, 266 abyssal zone, 69 algal stocks, 271 bathyl zone, 69 bathymetric divisions, 69 geographical divisions, 69, 70 teredinids, 424-425 tertiary level, 257 tuna (fourth) level, 257, 266

Deep water-continued ultra-abyssal zone, 69 vertical zones, 69 Deep-water acidians distribution, 69, 71-79 identification of species, 77, 79 zoogeographical divisions, 70, 79 Deep - water ascidians, geographical distribution, 69-79 depths greater than 2000m, 70-79 Deldeld’s haematoxylin, 382 Detritus, 34, 102, 108, 130, 132 diet for zooplankton, 130, 132 flocculent, 130 natural, 130 vegetable, 130 Deuteromycetes, 458 Diatoms, 4, 5, 112, 115, 117, 125, 129, 130, 132, 133, 138, 139, 141, 155, 156, 158, 159, 164, 167, 186, 188, 277, 407 neritic, 120 Diazonidtle, 16 Diazoninae, 63 Didemnidae, 15, 16, 37, 47, 54, 59, 69, 71 N-(D-2,3-Dihydroxy-n-propyl) taurine, 212 Dimethyltaurine, 212 Dinard, France, 35, 406 Dinoflagellates, 115, 126, 133, 188 “Discovery” Expedition, 64, 66, 256 Doboy Sound, 150, 153 Drake, 336 Dug-out canoes, 458

E Echinoderms, 61 taurine in, 210, 211 Elasmobranchia, 211, 227 English Channel, 36, 61, 105, 106, 129, 132, 137, 142, 155, 162, 318,406 Test Estuary, 150 Engraulidae, 274 Ensenada, 273 Enterocolidae, 52 Enterogona, 18 Epifauna, 44

547

SUBJECT INDEX

Equatorial Countercurrent, 261, 262, 263,268,284,285,288,292,293 Equatorial Current, 264, 296 north, 260, 261, 262, 263, 267, 285, 288, 291, 293, 320, 322 south, 261, 262, 263, 267, 268, 284, 291, 292, 293,296, 319, 320 Equatorial undercurrent, 261 Ernakulam channel, 420 Espegrend, Norway, 426, 450 Essex, 10 Eulrtmellibranchia, 348, 376 Euphausids, 129, 131, 302, 303, 304, 306, 309, 316 Euphausiids-mysids, 141,142, 144

Europe Atlantic coast, 346, 347 Euryhaline bivalves, 126, 238 taurine in, 236 Euryhaline carideans, 234

F Faeroes, 64 Falkland Islands, 65, 66 F.A.O. Yearbook of Fishery Statistics, 81

Fiji, 454 Firth of Clyde, 10, 40 Fish bathypelagic, 266, 276 community in an upwelling area, 274, 276

consumption by birds, 315 demersal, 290 distribution in upwelling areas, 314, 315, 316, 317, 318, 323, 324

plankton eating, 306, 307 production in upwelling axeas, 255326

spawning, 273, 274, 277, 311, 315, 316, 317, 318 Flagellates, 133, 407 Flatfish, 315 Flatworms, 50 turbellmian, 49 Flores Sea, 290, 298, 300, 319 Florida, U.S.A., 12, 34, 43, 319, 426, 426 Fort Lauderdale, Florida, 426

France, 416 Freetown, 278, 285, 302 Friday Harbour, 415, 425 Fucacem, 37 Fungal infestation of timber, 468 Fungi, 371, 458 Furcellariana, 37

G Gadidaa, 274 Galapagos Islands, 262,291,296 “Galathea” expedition, 266, 294, 296, 298, 425

Ganges, 340, 464 Gannets, 316 Gastropods, 49 opisthobranch, 49 prosobranch, 48, 472 taurine in, 239 Genoa, 34, 80 George River, 454 Ghana, 60, 288, 291, 293, 296, 302 Gonostomatidaa, 274 Gorgonians, 41 Greenland, 62, 64, 346, 347 Grey Seal, 50 Guanape Islands, 284 Guano birds, 315, 319 Guano islands, 319 Guine~,60, 285, 287, 319, 325 Guinea Current, 285,287,288,302 Guinea Dome, 288, 291, 293, 296, 300, 320

Gulf Coast, 415 Gulf of Caxiaco, 293 Gulf of Cintra, 285 Gulf of Guinea, 285 Gulf of Lions, 46 Gulf of Maine, 108, 137, 142, 150, 168, 174, 176

Gulf of Mexico, 344, 346, 347 Gulf of Nicoya, 276, 293 Gulf of Panama, 271,276,277,293,425 Gulf of Tehuantepec, 276, 293 Gulf of Thailand, 298, 299, 300 Gulf of Venezuela, 293 Gulf Stream, 160, 153, 257 Gullmar Fjord, Sweden, 7, 45 Guyana, 479

548

STTBJEUT INDEX

H Haddock, 48 Haifa, Israel, 80 Hake, 273,274,276,277,309,316,316, 324 Pacific, 273 Hawaii, 268, 346, 347, 396, 417, 427, 430, 447, 449, 471, 480 Hawkesbury river, 464 Heard Island, 67 Herbivores, 310,311,314,317,318,323 Herring, 266, 276 Hexacrobylidae, 76 Hirtshals, Denmark, 416 H.M.S. “Owen” cruise, 289 H.M.S. “Triton”, 426 Hobart, Tasmania, 460 Holland, 416, 429, 479, 480 wooden dykes, 336 Holotrichs, 469 Homer, 336 Honsyu Island, 68, 63, 81 Horn of Africa, 268, 288 Hydroids, 41, 64, 80, 429 Hydromedusae, 141, 142 Hypobythiidae, 72 Hypotaurine, 206, 207, 208, 209, 217, 218, 219, 220, 221, 222, 223, 227, 232, 241 Hypotaurocyamine, 206, 209 phosphate, 209 Hysterocinetidae, 469

I Iberian coast, 286 Iceland, 62, 64, 416 Iglooik Island, 184 India, 337, 342, 343, 346, 347, 410, 416, 416, 429 Indian Ocean, 67, 68, 68, 69, 70, 77, 266, 267, 260, 280, 288, 289, 293, 294, 296, 296, 297, 298, 299, 301, 302, 306, 309, 337, 342, 343, 344, 419 Indian Ocean Islands, 342, 343, 346, 347 Indian peninsula waters, 66 Indicative World Plan (I.W.P.), 266

Indonesia, 288, 298, 299, 300, 306, 309, 342, 343, 346, 347, 481 Ingolf Expedition, 63 Inter-American Tropical Tuna Commission, 276 International Indian Ocean Expedition, 296, 298, 302 Irish Sea, 104 Inningu Sea, 107 Isethionic acid, 208, 224, 230 Isopods, 469 Ivory Cowt, 288, 291, 293

J Jamaica, 27 Japanese waters, 66, 66, 67, 68, 80, 81, 296, 320, 346, 347, 404, 406, 416, 430, 449 brackish ponds, 34 Java, 290, 293, 298, 299, 300, 301, 308 Java Dome, 300 Jelly fish, 306 Jouannetiinae, 348 Juday nets, 301, 302

K Kamchatka Peninsula, 63 Kattegat, 42, 62, 462 Kerguelen Island, 67, 68 Kingston Harbour, Jamaica, 12, 80 Kodiak Island, 274, 316 Korean waters, 81 Kristineberg, 448, 469 Kuphinae, 338 Kuril-Kamchatka Trench, 69, 76 Kuroshio current, 267, 296, 320

L La Jolla, 165 Lacrinae, 64 Ladysmith Harbour, 460 Lake Maracaibo, Venezuela, 466 Lamellariacea, 49 Lamellibranch, 346, 387 Laminarians, 37 Lemon sole, 48

SUBJEUT INDEX

Lichomolgidae, 62 Licnophoridae, 469 Littoral fauna, 46, 68 Lobsters, 474 amino acids in, 213 Loch Ryan, 417, 419, 424, 467 Long Island Sound, 108, 109, 129, 141, 142, 146, 160, 162, 162, 166, 187, 188, 189, 191, 192 Luderitz, 311

M Mackerel, 276 horse, 316 jack, 273, 274, 276 Macquarie Island, 67 Madagascar, 289, 296, 298, 300, 319, 320, 342, 343, 346, 347 Madras, India, 12, 339, 341, 406, 414, 427, 460 Magellanic Islands, 66 Malabar coast, 266, 267, 264, 288, 299, 300, 319 Malay archipelago, 68 Malaysia, 342, 343 Malpique Bay, 404 Manati Bay, Cuba, 417, 419 Mangroves, 466, 474 attack by shipworms, 474 Marbat, 279 Marine borers (see Shipworms) “Marine Fouling and its Prevention”, 79 Marine invertebrates, 205-241 Marine invertebrates, amino acids in, 221, 228, 229, 230, 231, 232, 233, 234 concentration in nerves, 229 concentration in tissues, 221, 231, 232,233,234,236,236,237, 238, 241 effect of increasing salinity, 232,233, 234, 236, 236, 237, 240 isosmotic intracellular regulation, 233,234, 236, 236,238,240 osmotic balance, 229, 230, 231, 232, 233, 234, 236, 236, 238 synthesis and breakdown, 237,238

549

Marine invertebrates, t a u r i n e in, 205241 Annelida, 209, 211, 239 Arthropoda, 211 Brwhiopoda, 206,211, 212 Bryozoa, 212 chemistry, 216-227 Cnidaria, 206, 211 coelenterates, 212, 226 Crustacea, 209,210,212,224,233 cuttle&h, 211, 228 decapods, 233 distribution, 215 Echinodemata, 210, 211, 212 effect of salinity, 232, 233, 234, 234, 236, 237, 240 effect on nerve function, 238, 239 euryhaline bivalves, 236 formation, 219, 220, 221, 222, 223 function, 227-240 gastropods, 239 intracellular isosmotic regulation, 233, 234,236,236,238,240 lobster muscle, 213 minimum and maximum concentrations, 211 Mollusca, 207, 208, 209, 211, 224, 231, 232, 239 octopus, 229 osmotic balance, 229, 230, 231, 232, 233,234,236,236,237,238,240 oysters, 211, 228 phoronids, 231 “poikilosmosity”, 233, 236 polychaetes, 212, 213, 224, 226, 231 Polyzoa, 206, 211 Porifera, 206, 211 prosobrmchia, 233 regulation of intercellular osmotic pressure, 229, 230, 236, 238, 240 Sipuncula, 206,224, 226, 231 sponges, 220, 226, 227 Tunicata, 210, 212 Marine sediments, 106 Marquesas divergences, 268, 300, 307 Marqueeas Islands, 292,319 Marseilles, 26, 41, 460 M&ssachusetts,416, 474 Mazagm, 286

660

SUBJEUT INDEX

Mediterranean, 8, 24, 34, 39, 42, 55, 56, 60, 61, 62, 69, 81, 255, 344, 447 Mesogastropods, 40 “Meteor” expedition, 255,256,302,306 Methionine, 216,217,219,222,223,232 Mexico, 271, 294, 318, 344 Miami, Florida, 406, 417, 426 Miami river, 424 Microzooplankton, 159, 161 nutrient excretion, 161 Midway Islands, 346, 347, 447 Milford, 450 Millport, Scotland, 9, 10, 23, 26 Miraflores Lake, Panama, 456,457 Mississippi, 319, 456 Molgulidae, 16, 18, 34, 38, 39, 65, 75 Molgulids, 34, 39, 47, 65 MoIluscs, 48, 49, 53, 54, 67, 81, 212, 230, 306, 307, 386, 391, 411, 419, 431, 434, 435, 436, 438, 458, 460, 462, 466, 472 as hosts of zooparasites, 467 gastropod, 54 mode of attack of wood, 466 nudibranch, 49 taurine in, 207, 208, 209, 211, 212, 220, 224, 231, 232, 239 Monomethyltaurine, 206, 212 Monterey, 273, 275, 276, 277 Morrumbene, 68 Mouta Secca Point, Congo, 425 Mozambique, 289 Mud snails, 142 Mussels, 53, 54, 80, 464, 469 Myacea, 365 Myctophidae, 274 Myctophids, 256, 257, 307

N Nanoplankton, 381, 443, 444 amino acid composition, 444 Nantucket, 319, 320, 321 Naples, 9, 24, 34, 42, 48 Narragansett Bay, 107, 150, 156, 160, 162, 186, 186

Natural marine communities euryhaline species, 121 eutropic, 120 oligotrophic, 120

Nauplii, 302, 303, 304, 306 Nauva river, 464 Nematodes, 5 Nemertines, 54 Nevada, 271 New England coast Waters, 108, 173, 174, 175

New Guinea, 291,296,300,319 New Haven, Connecticut, 396 New Jersey, U.S.A., 40, 406 New South Wales, 33, 481 New York, 145, 460 New Zealand, 33, 53, 66, 67, 68, 294, 296, 342, 343, 346, 347

Newfoundland, 168 Newport, Rhode Island, 474 Nieuport, Belgium, 480 Nitrogen effect of nutrient levels on phytoplankton growth kinetics, 122126

excretion by zooplankton, 145-152, 166-160

in Atlantic Ocean, 103 in Irish Sea, 104 in marine biocycle, 103 in Pacific Ocean, 103, 104 levels in phytoplankton, 126-128 levels in zooplankton, 140-145 micro-Dumas determination, 140 micro-Kjedahl determination, 140, 146

release of organic forms by phytoplankton, 127-128 seasonal variation off New England coast, 173, 174 uptake by phytoplankton, 113-121 Nitrogen, assimilation by zooplankton, 128-140

detritus, 130 dissolved organic material, 130-132 laboratory studies, 132-136 living diets, 129 superfluous feeding, 136-140 Nitrogen, chemical forms in sea, 102105

in organic, 103 organic, 104 physio-ohemical reactions, 104

661

SUBJEU” INDEX

Nitrogen, excretion by zooplankton, 145-152, 156-162

nutrient regeneration, 160-162 seasonal surveys, 156-160 Nitrogen-fixingorganisms, 103 Nitrogen, in growth of zooplankton, 162-172 egg production, 165

net and gross growth efficiencies, 165-172

rate of growth, 162-165 Nitrogen, nutrient levels and plankton production, 172-192 partially enclosed sea arm, 185-192 polar regions, 182-185 seasonal variation, 173, 174, 181, 186, 187, 188, 189

temperate regions, 172-178 tropical and sub-tropical regions, 178-1 82

vertical distribution, 174, 184, 191 Nitrogen, stoichiometry of biologically induced changes in nutrient level, 106-113

apparent oxygen utilization, 109-1 13 “assimilation ratio”, AN: AP, 1 0 5 109,110,111,112

Nitrogen, uptake by phytoplankton, 113-121

effect of light, 116-117 hyperbolic relationship, 117-121 inorganic forms, 113-116 North America east coast, 346, 347 west coast, 346, 347 North Sea, 142, 267 Norway, 24, 26, 61, 415, 416, 447, 450 marine ponds, 42, 43 Norwegian Antarctic Expeditions, 65 Norwegian Sea, 142 Notodelphyidae, 51 Nova Scotia, 108, 258, 259,453,460 Bras #Or Lake, 150,153, 161 Morrison’s Pond, 150, 154, 161

0 Oahu, Hawaii, 417, 419, 454 Octachemidae, 72

Octopua taurine in, 229 Ohio, 475 Onagawa Bay, Japan, 450,451,453 Orange River, 279, 286, 311, 319 Oregon coast, 111, 260, 272, 273, 274, 325

Omund, 62 Oriesa, 290, 298, 299, 300, 308 Oslo Fjord, 120 Ostend, 20, 36 Ostrmods, 5 Ovid, 336 Oysters, 48, 50, 80, 337, 434, 435, 438, 439, 451, 456, 464, 469

culture, 81, 415 Olympia, 459 taurine in, 211, 228

P Pacific, 55, 56, 64, 68, 69, 70, 77, 79, 103, 104, 105, 107, 111, 116, 256, 257, 260, 261, 262, 267, 268, 271, 273, 291, 292, 293, 295, 296, 298, 300, 301, 302, 307, 310, 315, 319, 320, 322, 344, 415, 428 American, 61, 63 Indo-Malayan, 56, 57, 58 Indo-West, 56, 58, 60, 68, 340, 344, 428,430 north, 260, 263, 273, 320, 429 north-eastern, 57, 63, 116, 168, 429 north-western, 56,57,63,346,347 southern Japanese, 56, 57, 58 west, 344 Pacific Islands, 346, 347, 481 Pago Pago Harbour, 396 Pakistan coasts, 289 Panama Canal, 456, 457, 479 Pandanus fruit, 424 Panjim, 290 Patagonian Shelf, 4, 39, 66 Pelicans, 315 Penguins, 315 Peridineans, 5 Persian Gulf,342, 343 Peru, 61, 255, 256, 257, 284, 291, 296, 300, 308, 313, 314, 316, 318, 319, 454

552

SUBJECT INDEX

Peru Current, 256, 257, 267, 269, 278, 284, 285, 296, 300, 302, 305, 309, 311,314, 315,316, 319,320 “El Niiio”, 284, 285, 315 Philippine Islands, 58, 291, 296, 346, 430,447,474, 475 Pholadidae, 365, 370 Pholadinaa, 345, 348, 353 Pholads, 388, 410, 436 Phoronids taurine in, 231 Phosphorus determination, 140 distribution in upwelling areas, 267, 268,269,270,271,291,292,324 effect of nutrient levels on algae growth, 267 effect of nutrient levels on phytoplankton growth kinetics, 122126 excretion by zooplankton, 152-165, 156-160 in English Channel, 105 in Pacific Ocean, 106 levels in phytoplankton, 126-128 levels in zooplankton, 140-146 r e l w e of organic forms by phytoplankton, 127-128 uptake by phytoplankton, 121-122 ,Phosphorus, mimilation by zooplankton, 12&140 detritus, 130 dissolved organic material, 130-132 laboratory studies, 132-136 living diets, 129 superiluous feeding, 136-140 Phosphorus, chemical forms in sea, 102-105 inorganic, 106 organic, 105 Phosphorus, excretion by zooplankton, 162-165, 156-162 nutrient regeneration, 160-162 seasonal surveys, 156-160 Phosphorus, in growth of zooplankton, 102-172 egg production, 186 net and gross growth efficiencies, 166-172 rate of growth, 162-186

Phosphorus, nutrient levels and plankton production, 172-192 partially enclosed sea areas, 185-192 polar regions, 182-185 seasonal variation, 174, 175, 181, 186, 187, 188, 191 temperate regions, 172-1 78 tropical and sub-tropical regions, 178-182 vertical distribution, 176, 184, 189, 190,191 Phosphorus, stoichiometry of biologically induced changes in nutrient level, 106-113 apparent oxygen utilization, 109113 “assimilation ratio”, AN: AP, 106109 Phosphorus, uptake by phytoplankton, 121-122 inorganic forms, 121 organic forms, 121-122 Phytofiagellates, 132 Phytoplankton, 3,4,102,103,104,105, 106, 107, 108, 109, 112, 113, 116, 116, 117, 118, 121, 122, 123, 124, 125, 126, 127, 128, 129, 130, 132, 137, 138, 139, 140, 144, 148, 152, 156, 159, 160, 161, 165, 172, 174, 176, 177, 178, 180, 182, 183, 185, 187, 188,189,191, 192,447 cell growth, 123 cellular nutrient content, 123, 124 consumption by zooplankton, 136140 effect of nutrient levels on growth kinetics, 122-126 growth rates, 122, 123, 124, 126, 138 in Long Island Sound, 108, 109, 126 in Sargamo Sea, 11 6 in upwelling areas, 275, 276, 289 nitrogen and phosphorus levels, 109, 110.111,112,113,126-128,161, 166 production, 137 release of organic nitrogen and phosphorus, 127-128

553

SWJEOT INDEX

Phytoplankton, uptake of nitrogen compounds, 113-121 effect of light, 116-117 hyperbolic relationship, 117-121 in Caribbean, 116 in Pacific, 116 in Sargasso Sea, 116 inorghc forms, 113-116 Phytoplankton, uptake of phosphom compounds, 121-122 inorganic forms, 121 organic forms, 121-122 Piddocks, 346 Pilchards, 316, 318 Pisco, 311 Planarians, 478 Plankton, 6, 7,21,30,47,102, 104, 105, 106, 110, 112, 177, 181, 184, 186, 256, 266, 276, 283, 303, 307, 311, 312, 323, 369, 381, 404, 413, 414, 436, 443, 444 crustacean, 138 in nitrogen and phosphorus cycles in sea, 101-192 Plankton, production and nutrient levels, 172-192 partially enclosed sea meas, 185192 polar regions, 182-185 temperate regions, 172-178 tropical and sub-tropical regions, 178-182 Planktonic algae, 4 Pleurogona, 18 Pleuronectidae, 274 Pliny, 336 Plymouth, 13, 24, 36, 416 Point Barrow, Alaska, 34 Point Conception, 271, 272, 273, 278, 281, 316 Pointe Noire, 279, 287, 288 Polychrtetes, 48, 61, 64, 142, 184, 463, 478 association with shipworms, 472 taurine in, 212, 213, 224, 226, 226, 231, 240 Polycitorines, 30 Polyclinidae, 16, 16, 21, 30, 71 Polyclinids, 30 Polysiphonians, 37

Polyzoa aa protective cover of timber against wood-borer attack, 461, 462466 taurine in, 206, 211 Polyzoinae, 66 Port Gentil, Congo, 426 Port Jackson, 454 Portland, Maine, 481 Port0 Amboin, 279 Portobello, New Zealand, 12 Portugal, 286 Prosobranchia, 233 taurine in, 206, 211 Protozoa, 444 Protozoans, 367, 469, 478 association with shipworms, 469, 470, 471 parasitic, 469 Pteropods, 142, 304 Puerto Rico, 319 Puget Sound, 460 Pulicat Lake, 454 Punta Aguja, 284, 316 Punta San Eugenio, 272,273,316,318, 326 Punta San J u d c o , 272 Pyuridrte, 16, 33, 37, 38, 39,74, 76 PyLlrids, 37, 43, 44, 49

R Radiolarians, 4 Rdiolarian skeletons, 262 Radionuclides, 82 Rangoon, 416 Rangsit Canal, Thailand, 467 Ras al Hadd, 279 Ras aa Salala, 279 Ras Fartak, 279 Raa Mabber, 289 Red Sea, 64, 67, 69, 61, 69, 342, 343, 346, 347 Redfish, 276 Rewa river, 454, 466 Rhabdocoele turbellarian parasites, 47 1 Rosef%h, 276, 316 Rovigno d’ Istria, 401 R.R.S. “Discovery”, 301

664

SUBJECT INDEX

S Sarsnich Inlet, 150 Sacramento river, California, 467 Sagittas, 142 Saint Mato, 406 Saldanha Bay, 68 San Diego, 273, 315 San Francisco, 273, 336, 463, 460 San Juan Island, 150, 315 San Sebastih, 402 Sangor Island, 290, 298 Santa Elena, 284 Santa Margarita island, 293 Saramacca Canal, Dutch Cuiana, 479 Sardines, 273, 274, 277, 309, 316, 324 Californian, 309, 316, 316 South African, 309 Sargasso Sea, 113, 116, 120, 141, 142, 178, 179, 180, 181, 182, 312 Scallops, 459 Scombridae, 274 Scorpaenidm, 274, 276 Scottish coast, 11, 33, 34, 45, 65, 426 Scottish waters benthic survey, 34 Sea areas, plankton production and nutrient levels, 172-192 partially enclosed a r m , 186-192 polar regions, 182-186 temperate regions, 172-178 tropical and sub-tropical regions, 178-182 Sea of Japan, 65, 69, 143 Sea urchin, 238 isosmotic intracellular regulation, 238 Sea water apparent oxygen utilization, 109113 “brown water”, 311 compensation depth, 264, 265 depth of mixing, 264 detritus content, 130 dissolved organic material, 130-132 euphotic zone, 107, 110, 122, 128, 137, 161, 172, 174, 176, 177, 178, 180, 187, 192 inorganic nitrogen content, 103-104, 113-116

Sea water-continued inorganic phosphorus content, 106, 121 nitrogen: phosphorus ratio, 106-109 nutrient level, 106-113, 122-126, 172-192, 267 organic nitrogen content, 104 organic phosphorus content, 105, 121-122 oxidation of ammonia, 104 phosphorus turnover rate, 271 photic layer, 266, 266, 294, 312, 313 plankton production, 172-192 production cycle in, 264, 266, 266, 267 stock sampling nets, 301, 302, 303 temperate waters, 264, 265 upwelling in, 111, 125, 255-326 Sea water, nitrogen: phosphorus ratio, 106-109, 110, 111, 112, 113 a t different depths, 106 in Costa Rica dome, 111 in euphotic zone, 107 in Irminger Sea, 107 ih Long Island Sound, 108 in Narragansett Bay, 107 in Pacific Ocean, 107, 111, 116 of New England coast, 108 seasonal variation, 108, 109 Sea water, plankton production and nutrient levels, 172-192 partially enclosed sea meas, 185-1 92 polar regions, 182-185 seasonalvariation, 173,174,175,179, 180, 181, 182, 183, 186, 187, 188, 191 temperate regions, 172-178 tropical and sub-tropical regions, 178-182 variation with depth, 172, 174, 176, 176,177,178,183,184,189, 190 191 Sea water, stoichiometry of biologically induced changes in nutrient levels, 106-113 apparent oxygen utilization, 109-113 “assimilation ratio”, AN: AP, 106109 Sabmtopol, 396

SUBJEUT INDEX

Senegal, 296 s088ile communities, 80 Shag Rook Bank, 64 Shallow-water ascidians, geogmphical distribution, 68-69 Antarctic, 6 P 6 6 Antiboreal, 66-66 Antiboreal (subantarctic) islands, 67-68

Antiboreal South America, 66 Arctic, 63-64 Boreal American Atlantic, 62-63 Boreal European Atlantic, 61-62 Indo-Mdaya, 68 Indo-West-Pacific,66 Mediterranean, 60-61 north Australia, 69 northeast Australia, 69 north-west Australia, 69

Red

Sea, 69

South Africa, 68 southern Japan, 66-68 subtropical American Atlantic, 60 subtropical American Pacific, 61 subtropical West Africa, 69-60 temperate north-eastern Pacific, 63 temperate north-western Pacific, 63 tropical American Atlantic, 60 tropical American Pwific, 61 tropical West Africa, 69-60 western Indian Ocean, 68-69 Shipworms (see also Teredinidae) age or size a t sexual maturity, 396 association with cmtacean borers, 466, 467

biology, 335-482 brackish-waterspecies, 391,428,429, 464, 466, 474

breeding season, 394, 396-399, 409, 410,411,416,431,434,436,436, 437,438,439,447,448,449,460, 461, 463

detection and prevention of attack, 475-478 dispersal, 428-431, 461, 462 distribution in Atlantic Ocean, 344, 346, 347 distribution in Indian Ocean, 342, 343, 344, 346, 347

666

Shipworms-wntind distribution in Mediterranean, 344, 346, 347

distribution in 'Pacific Ocean, 344, 346, 347

ecology, 446-474 embryology and lava1 development, 401-409, 448

estuarine forms, 397, 410, 414, 418, 419,420,426,427,436,438,462, 460 fecundity, 396 fertilization, 399-401, 402, 403 freshwater forms, 466-467 food and digestion, 441-446, 460 genera, 338, 340 growth rates, 426-428,449,460,461, 472,476 history of damage, 336, 337 in deep water, 424-426 mode of attack of wood, 466, 467, 468 morphology and anatomy, 344-390, 434 nut-infesting species, 430 objects attacked, 47-75

pattern of distribution along Indian coasts, 339, 340, 341, 342

pattern of vertical settlement, 417424, 461

physiological studies, 431-440 predators, 471, 478 season of settlement, 409-417, 419, 420, 423

sexual phases, 390-396 species, 340, 341, 342, 343, 344, 346, 346, 347

stenomorphic forms, 360 taxonomy, 346, 364, 366, 369, 360, 366, 469

timbers of unusual durability'against attack, 478-482 Shipworms, breeding w o n , 396-399, 409, 410, 411, 416, 431, 434, 436, 436, 437, 438, 439, 447, 448, 449, 460, 461, 463 effects of salinity, 463, 464 effects of temperature, 447, 448, 449, 460, 461,462,463 gonad indioea, 397,398,399,411.434

656

SUBJEaT INDEX

Shipworms, breeding season -continued methods of determination, 396, 397 reproductive cycle, 397,399 sexual activity, 449 spawning, 397, 399, 401, 402, 410, 434,438, 439,449,460, 461 Shipworms, ctenidia, 376-381 demibranchs, 376, 378 function, 380, 381 gill lamellaa, 378, 379, 380, 381, 382, 384

homorhabdic branchial filaments, 376

nature, 376 Shipworms, detection and prevention of attack, 476-478 biological control, 478 “Carbo-Teredo” process, 476 desiccation, 476, 476 detonating, 476 divers, 476 electrical stethoscopes, 476 electrocution, 477 electrolytic protection, 476 exposure to fresh water, 476 microphones, 476 preservation with creosote, 477 sonic testing, 477 scupper nailing, 476 sheathing, 476 stereo-radiography, 476 rise of poisom, 476, 477 rise of predators, 478 X-ray photography, 476 Shipworms,dispersal, 42&431,461,462 effects of salinity, 428 effects of temperature, 429 in floating wood, 429, 430, 451 in new areas, 428 in ships’ hulls, 429, 430, 461 through larval stages, 428, 429, 430 with long-term larviparous young, 428,429

with oviparous young, 428 with short-term l a r v i p a r o ~young, ~ 428, 429

shipworms, ecology, 446-474 effectsof illumination on settlement, 467

Shipworms, ecology-contind effects of marine fouling, 461, 463466

effects of marine fungi on attack of Wood, 458-469 effects of oxygen content of water on attack, 469-460, 461, 462 effects of pollution, 460-462 effectsof salinity, 447, 448, 462-466, 466,467

effects of salinity on developing eggs, 466

effects of turbidity, 460 effects of water currents on rate of attack, 469 growth rates, 449, 460 hydrogen-ion tolerance, 460 influence of temperature on activity and distribution, 447-452, 466 limitation in geographical range, 462 occurrence in fresh water, 466467 parasites and associates, 467474, 478

relation to other borers, 466467 role of primary film in settlement, 467-468

salinity tolerance, 462, 463, 454, 466, 466

settlement in relation to light and gravity, 467, 468 spawning activity, 460, 461 spawning temperature, 460, 461 temperature tolerance, 448,449,460, 461, 462

Shipworms, embryology and larval development, 401-409, 448 boring stage, 406 crawling stage, 404, 406, 409, 440, 467

development stages, 402406 duration of larval period, 406 effects of salinity, 448, 466, 466 effects of temperature, 447, 448, 449 food of larvae, 407 free-wpiUrming stage, 400, 402, 404, 406,409,410,428,429,430,449, 467 gametes, 401-402, 431, 448 metamorphosis, 406 pediveliger, 406

667

SUBJlOT INDEX

Shipworms, embryology and larval development-contind pelagic life, 404, 451 penetration of larva into wood, 408, 409

planktotrophic life, 428 salinity tolerance, 456 settlement on wood, 404, 405, 406, 407-409,410,411,412,413,457, 458, 459, 463 straight-hinge larva, 403 swimming rates, 406 trochophore larva, 403 two-celled Stage, 400, 402 veligers, 400, 403, 404, 405, 406, 413, 414, 428, 429 velum, 400, 403, 405 Shipworms, fertilization, 399401, 402, 403 artificial, 402 extrusion of larvae, 401 modes, 399,401 stages of development, 400,402,403, 404 Shipworms, food and digestion, 441446, 460 bacteria, 442, 445, 446 breakdown of cellulose, 441,442,443, 445,446 carbohydrates, 441, 442, 443 effects of fungi, 445 effects of harmful bacteria, 444 effects of overcrowding, 444 effects of parasitic protozoa, 444 excavated wood, 441, 442, 444, 445 nanoplankton, 443, 444 phagocytosis, 445 plankton, 443, 444 presence of cellulose enzyme, 441, 442, 443, 445, 446 storage of glycogen, 443,459,460 Shipworms, growth rates, 425428, 449, 450, 451, 472, 475 effects of overcrowding, 426,427,428 effects of salinity, 427, 428 effects of temperature, 449, 450, 451 rate of boring, 425, 426 “stenomorphs”, 426, 427 sterioradiographic studies, 425 X-ray photographic studies, 425

S h i p ~ ~ r mmantle, s, 351-359 calcareous tube, 357 calcium carbonate secretion, 355 “cephalic hood”, 355 cilia, 358,359 epithelium, 357, 358, 359 periostracal groove, 357 structure, 355, 356, 357, 358 Shipworms, morphology and anatomy, 344-390, 434

adductor muscles, 348, 350, 351, 354, 369, 366, 367,385, 386,400

alimentary canal, 348, 367, 368,441, 443

anal canal, 349, 350, 368, 369, 376, 377, 378, 386

anterior adduction, 349, 350, 353, 354,359, 368,377,378,388,400

anterior aorta, 349, 350 anus, 349, 368, 377 aorta, 384, 385 appendix, 370, 371, 376, 389, 390, 441, 445

arrangement of organs, 349,350 auricles, 349,368,377,378, 385, 387, 390

body, 345, 348, 349, 367, 374, 376, 383, 385, 388, 428

boring mechanism, 365-367 branchial cavity, 349, 358, 376, 378, 382, 383, 389, 390, 469, 472

brood pouch, 368, 377, 401 caecum, 349,360,360,368,369,370, 371, 374,376,377,378,379,389, 390,400,441,442,445,446 calcareous lining, 363-365 cephalic hood, 349, 366, 378 cerebral ganglia, 388, 389 circulatory system, 38P386 coiled typhlosole of intestine, 349, 368, 377, 445 collar, 350, 351, 363, 377, 378 collar of mantle, 349 ctenidia, 349,350,357,359,376-381, 382, 386, 390, 470 digestive diverticula, 349, 350, 368, 371, 372,373,374,377,378,381, 400, 441, 442, 443, 445 digestive 8JTstem, 367-376

658

SUBJXX INDEX

Shipworms, morphology and anatomy --continued epibrmchial cavity, 377, 378, 383, 387, 389, 399

excretory system, 386-387 exhalant siphon, 349, 351, 364, 365, 368,377, 378, 399,400, 472 foot, 348, 350, 366, 368, 373, 376, 371, 378, 388,400, 403,404,405, 406, 409, 443 gills, 349, 358, 368, 377, 378, 379, 380,381, 382,383,384,385, 389, 400,401,404,406,440,469,470 glands of Deshayes, 380, 381-384 gonads, 350, 368, 377, 378, 389, 390, 391, 392,394,395,397, 398, 399, 413,431,432,434, 436,449 gut, 349,368, 369, 371, 315, 376, 377, 378, 400, 441, 443, 445 heart, 349, 360, 384, 385 inhalant siphon, 349, 351, 364, 365, 368, 377, 378, 399,400, 440 intestine, 349, 350, 360, 369, 370, 316, 384, 385, 400, 441 kidney, 349, 350, 368, 377, 378, 386, 387 labial palps, 349, 368, 369, 371, 376 “liver”, 441 lumen of gut, 445 mantle, 351-359, 366, 377, 379, 387, 390, 438, 440, 469 mantle cavity, 349, 350, 351, 368, 376,378,389,400,401,429 mouth, 349, 368, 377, 378, 381, 384, 388, 400 nervous system, 388-389 neuro-secretory cells, 388, 389 oesophagus, 368, 377, 383, 384, 388 ovary, 349 oviduct, 349 pallets, 348, 350, 351, 355, 359-363, 364, 427, 428 pedal ganglion, 388 pericardid cavity, 350, 389 pericardium, 349,350,368, 377, 384, 385, 386, 387, 390 posterior adductor, 349, 350, 353, 354, 359,368,377, 385,386,400 posterior aorta, 350 rectum, 349,368,377,378,400,441

Shipworms, morphology and anatomy --continued renal duct, 349, 371, 386, 387, 388 reproductive system, 389-390 shell, 348, 349, 351-359, 366, 381, 400,403,404,406,409, 427,443, 45 1 siphons, 348, 349, 350, 351, 355, 357, 359, 363,364, 365, 376, 377,401, 405, 465, 466, 475 stomach, 349,350,368,369,371,373, 374,376, 317,400,442,445 style sac, 368,369,375,377,400,441, 442, 443, 445 typhlosole, 370, 371, 375, 376, 377 ventricle, 349, 350, 368, 377, 378, 384, 385 visceral maw, 348,349,358,376,385, 440 visceral ganglion, 349, 350, 368, 377, 378, 386, 387, 389, 390, 400 Shipworms, objects attacked, 474475 buoys, 414 cable covers, 474 cork, 474 docke, 474 floats, 474 mangroves, 474 wooden hulls, 474 Shipworms, pallets, 359-363 evolution, 360, 361, 362 growth, 362 mechanism, 360 non-segmented, 360, 361, 362 periostracal cap, 360 segmented, 360, 361 role in clamification, 359, 360, 362 variations, 360, 361

Shipworms, pattern of vertical settlement, 417-424, 451 at intertidal level, 412, 413, 419 at mud line, 417,419, 421, 422,457 at sub-tidal level, 412, 413, 419, 421 at surface, 417, 419, 420, 422, 423, 467

deterioration of wood piles, 417 distribution of larvae, 419, 421, 422, 424

effects of gravity, 457

659

SUBJE43” INDEX

Shipworms, pattern of vertical settlement-oontitwed effects of light intensities, 424, 467, 468

effects of marine fouling, 461, 462466

effects of monsoon periods, 412, 413, 419, 420, 421, 422

effects of salinity, 419, 420, 421,422, 423, 424

effects of temperature, 420 effects of water currents, 469 in shallow waters, 419, 423 on bottom, 412, 413, 419, 421, 422, 423, 424

role of primary film on wood, 468 test panels, 417, 421, 422, 424 Shipworms, physiological studies, 431440

amino acid composition, 444 rtnnud reproductive cycle analyses, 431,432,433,434,436,436,437, 438,439 ash content, 431, 432,433, 434, 438, 439 average day weight, 432, 436, 438, 437, 438 average monthly gonad index, 432, 434 average monthly salinity, 432, 434, 438 calcium content, 431, 432, 433, 434, 438, 439, 440 ohemical composition, 431 chloride content, 431, 432, 433, 434, 438 glycogen content, 431, 432, 434,436, 436, 437, 438, 440 glycogen distribution, 431 lipids content, 431, 432, 433, 434, 438 nitrogen distribution, 431 non-protein nitrogen oontent, 431, 432, 434, 437, 440 oxygen consumption, 440 phosphorus content, 431, 432, 433, 434, 439, 440 protein content, 431, 432, 434, 436, 436, 437, 438, 439 respiration, 440

Shipworms, physiological studies -continued t o t d nitrogen content, 431,432,433, 434,436, 436, 438, 440,443

water content, 431, 432, 433, 434, 439

Shipworms, season of settlement, 409417, 419, 420, 423

at Cochin harbour, 410,411,412,413, 418

at different localities of world, 416 effects of monsoon periods, 410, 411, 412, 413, 417

effects of salinity, 410, 411, 414, 417 effects of temperature, 410, 416, 417 number of generations, 416 test blocks, 411, 412,413,414 Shipworms, sexual phases, 390-396 ambisexual males, 391, 393, 394 bisexual males, 391 females, 390, 391, 393, 394, 396 hermaphrodites, 390, 391, 392, 393, 396, 396, 402

males, 390, 391, 394, 431 protandrous species, 390, 391, 393 self fertilization, 391, 394 true males, 390, 393 Shipworms, shell, 361-369 anterior, 362, 363, 367 anterior median, 362, 364 apophysis, 362, 363 auricle, 362, 369 dorsal condyle, 362, 363 middle median, 362 posterior median, 362, 363 structure, 361, 362, 363 umbonal-ventral ridge, 362, 363 use in clrtfKlification, 364, 366 valves, 361, 363, 364, 366, 369 ventral oondyle, 362, 363 Shipworms, timber durable against attack, 47-82 acapu, 480 beech, 481 Bitter Angelims, 480 effects of bark of trees, 481-482 ekki, 480 greenheart, 479, 480

hemlock, 481 Huon Pine,480

560

BWJECT LNDEX

Shipworms, timber durable against attack-continued inert properties of timber, 478, 479, 480 iron wood, 480 jarrah, 479 mahogany, 481 olive, 479 prickly tea, 481 role of silica, 480-481 sen, 481 teak, 479, 480 turpentine, 479, 481 yellow pine, 479 Sicily, 450 Sinepuxent Bay, U.S.A.,32 Siphonophores, 141, 142, 144 Sipuncda taurine in, 206, 224, 226, 231 Skagerak, 42 Snails, 49, 446 Socotra Island, 258, 289 “Soft rot” of wood, 458 Somali Current, 257,258,264,288,289, 296, 298, 300, 319, 325 South African waters, 57, 67, 68, 69, 286, 298, 315, 319, 320,429,430 South American waters, 57, 65, 67, 82, 429,481 east coast, 346, 347 west coast, 346, 347 South China Sea, 298 South East Asia, 346, 347 South Georgia, 64, 65, 66 South Orkney, 64 South Sandwich Islands, 64 South Shetland, 64 South Vietnam, 290 Southern Arabia, 266, 279, 296, 298, 299, 300, 301, 308, 319 Southern Ocean, 264 Spain, 286, 450 Spirostomidae, 469 Sponges, 79 taurine in, 220, 226, 227 Squids, 306, 307, 309 taurine in, 223, 224, 228, 230 St&h, 48 Stentoridae, 469 Strait of Georgia, 453

Straits of Gibraltar, 60 Styelidae, 16, 38, 39, 72, 73, 74 Styelids, 39 Sub-Antarctic, 64, 66, 67, 68, 182 Sub-Arctic, 24, 26 Sublittoral fauna, 34, 42, 46 Sublittoral sand, 18 Subtropical anticyclones, 257, 268, 266 Suez, 42 Sulu Sea, 426 Sumbawa, 293, 298 Sundepbans, 340 Swansea, Wales, 24, 44, 452 Sweden, west coast, 24

T Table Bay, 477 Taurine (2-aminoethanesulphonicacid) formation, in animals, 215, 216, 217, 218, 219 formation in marine invertebrates, 219, 220, 221, 222, 223 in algae, 212, 239 in amphibia, 227 in bacteria, 212 in bile of ox, 205 in bile of snakes, 227 in bile of teleosts, 227 in bivalves, 222, 232 in cat tissues, 218 in chick embryos, 223, 224 in cow tissues, 211 in dog tissues, 218, 224, 230 in dog urine, 226 in elasmobranchs, 227 in hens, 223 in marine invertebrates, 205-241 in rabbit tissues, 217 in rat tissues, 206, 215,217,218. 219, 222, 224, 230 in rat urine, 220, 226 in squid, 223, 224, 228, 230 in xenic cockroaches, 222 metabolic pathways in animals, 216 Taurine, in marine invertebrates, 205241 chemistry, 215-227 distribution, 215 formation, 219, 220, 221, 222, 223

661

SUBJECT INDEX

Taurine, in marine invertebrates --continzLed

function, 227-240 minimum and maximum concentrations, 211 regulation of intercellulm osmotic pressure, 229, 230, 236, 238, 240 Taurobetaine, 206, 224, 227 Taurocyamine, 206, 209, 224, 226,226,

Trematodes, 472 Tristan da Cunha, 67 Trivandrum, 290 Trondheim, Norway, 416, 426, 460 Tuna, 300, 316, 320, 322, 323 Tunicata taurine in, 210, 212 Turbellarians, 471,472

227

phosphate, 209, 226, 226 TeUinacea, 370 Tehuantepequeros winds, 293 Teredinidae (see also Shipworms) age or size a t sexual maturity, 396 boring mechanism, 366, 366, 367 brackish water genera, 366 breeding season, 398-399 classification of genera, 338, 340 detection and prevention of attack, 476-478

dispersal, 428-431 I X O ~ O ~ Y ,446-474

embryology and larval development, 401-409

fecundity, 396 fertilization, 399-401 food and digestion, 441-446 growth rates, 426-428 in deep water, 424-426 mangrove genera, 366 morphology and anatomy, 344-390 objects attacked, 4744176 pattern of vertical settlement, 417424

physiological studies, 431440 rock-dwelling species, 469 season of settlement, 409417 sexual phases, 390-396 systematics and distribution, 338344

taxonomy, 338 timbers of unusual durability against attack, 478482 Teredininae, 360 Teredo (see Shipworms) Thailand, 290 Thermoclines, 290, 292, 316, 316 echo traces, 314 Thigmophryidae, 469

U Upper Pedro Miguel Locks, Panama Canal, 466 Upper Passau River, New Jersey, 467

Upwelling, 111, 126, 266-326 and production of fish, 265-326 biological system, 273, 274, 276, 276, 311-318

charting, 318-326 distribution and divergencies in anticyclones of an ocean, 260, 261, 262, 263, 264

distribution of sperm whales, 319, 320,321

dynamic model in biological terms, 314

effects of winds, 267, 268, 269, 260, 264,271, 272,273,276,284,286, 288,289, 290, 293 Ekman offshore transport, 260, 263, 311, 312, 316 future research, 326, 326 geostrophic, 264, 288 phosphatic deposits, 290, 318, 319, 320,321 physical background, 267-264 role of vorticity, 260, 264 seasonal cycle, 263, 272, 273, 282, 286,286,287,288,289,290, 292, 293, 298, 301 thermoclines, 290,292, 314, 316,316 Upwelling, biologicalbackground, 264271, 311-318 part played by nutrients, 267-271

production cycle in an upwelling area, 264-266 radiocarbon estimation, 263, 271, 276,277,291,294,296,297,298, 299,304,306,306,311,316,326

562

SUBJECT INDEX

Upwelling, charting, 318-326 distribution of guano islands, 319,

Upwelling areas-continued production of living material, 294311

321

phosphatic deposits, 318, 320, 321 sperm whale catches, 319, 320, 321 Upwelling, description of well known areas, 271-279 California Current system, 271-276 Gulf of Panama system, 276-277 Upwelling areas, 280-294 biological boundary, 266, 289 biology, 311-318 California Current system, 271-276 community structure, 266, 318 convergences, 269, 260, 261, 263, 264, 286, 292, 322, 323

divergences, 266, 268, 269, 260, 261, 262, 263,264, 266,284,286, 289, 291,292, 316, 319, 320, 322, 323, 324

domes and eastern boundary currents, 292-293 dynamic boundary, 269, 266, 323 ecological efficiency, 310 equatorial system, 291-292 Gulf of Panama system, 276-277 harmonic regression of temperature with date, 281, 282 in Eastern boundary currents, 284288

Indian Ocean, 288-290 living material transfer coefficients, 310-311

major upwellings, 278, 279 mean temperatures, 280, 281, 283, 287

minor upwellings, 293-294 part played by nutrients, 267-271,

“roller bearing”, 269, 260, 286 satellite photographs, 291 secondary living material production, 301-306, 308, 310, 311, 324,326

surface phosphate-phosphorus, 266 tertiary living material production, 306-310, 324

third trophic level living material production, 306-310, 323 vertical section, 269 width of upwelling zone, 281-284 zooplankton distribution, 267, 268, 269,270, 271, 277,282, 283,291, 292, 294, 311, 317, 324 zooplankton production, 301-306

Upwelling tmae in eastern boundary currents, 266, 284-288, 292,-293 Benguela Current, 286-288 Canary Current, 286-286 Peru Current, 28P286 Upwelling areas, production of living material, 294-311 a t third trophic level, 306-310, 323 cycle of production, 264-266, 310, 311, 312, 313, 314, 318

primary production, 294-301,

306, 306, 308, 310, 311, 324 secondary production, 301-306, 308, 310, 311, 324, 326 tertiary production, 306-310, 324 transfer coefficients, 310-311 zooplankton, 301-306 Urceolaridae, 469 U.S.N.S. “Eltanin”, 39

324

V

phosphorus distribution, 267, 268, 269, 270, 271, 291,292,324

photic layer, 266, 266, 312, 313 physical boundary, 281 phytoplankton outburst, 276 primary living material production, 29.4-301, 324

306, 308, 310, 311,

production cycle, 264-266, 267, 310, 311, 312, 313, 314, 318, 323, 324

Valparaiso, 284, 461 Vembarad Lake, 418 Venezuela, 293, 319 Venice, 9, 44, 47 Vietnam, 298, 299, 300, 319 Vigo, 278, 286 Visakhaptanam Harbour, 341, 396, 410, 469

419,

427,

460,

T i t y a z ” expedition, 296

463,

467,

668

SUBJEOT INDEX

w Wdthair, 290 Wdvis Bay, 279 Washington, U.S.A., 26, 271, 272, 273, 274, 318

West Afrioa, 67, 59, 291 West Bengal, 339, 340, 454, 474, 476 West Indies, 66, 60, 474 West Wind drift, 272 Whales, 316 grey, 320 sperm, 319, 320, 321 Wilmington, 416, 426 Wood-boring teredinid molluscs (see also Teredinidae; shipworms) biology, 336-482 Woods Hole, 396, 406, 426, 474 World Atlas of Sea Surface Temperatures, 280

Zoophkton-continued distribution in upwelling areas, 267. 268,269, 270, 271, 277, 282, 283, 291, 292,294,311, 317, 324 diurnal vertical migration, 171 faecal pellets, 130, 132, 133, 134, 136, 136, 137, 138, 147, 149, 164, 169, 170 free amino acid content, 131, 136

growth in terms of nitrogen and phosphorus, 162-172 in Sargasso Sea, 113, 141 levels of nitrogen and phosphorus, 113, 140-146, 161

nitrogen excretion, 146-162,156-160, 174, 191

nutrient regeneration, 160-162 phosphorus excretion, 162-166, 166160, 177, 180

production in upwelling areas, 301-

X Xylophaginidae, 348, 366

Y Yokohama, Japan, 481 Yucatan, 294, 319

Z Zembezi River, 464 Zoo-parasites, 467 Zoochlorellae, 64 Zooids, 14, 16, 19, 27, 29, 30, 31, 48, 60 Zooplankton, 102, 104, 106, 113, 128, 129, 138, 146, 164, 164, 178, 188,

130, 131, 132, 136, 136, 137, 139, 140, 141, 142, 143, 144, 147, 149, 160, 161, 162, 163, 166, 166, 169, 160, 161, 162, 166, 166, 169, 170, 171, 172, 180, 181, 184, 185, 186, 187, 189, 191, 192, 267, 266, 267 algal diet, 129, 136, 146 capture, 137 cast moults, 130

determination of nitrogen content, 140-145

determination of phosphorus content, 140-146 digestion of phosphorus, 132, 133, 134, 136

306

respiration rate, 138, 139 sampling by nets, 302 seasonal changes in nitrogen and phosphorus content, 140-146 seasonal variation, 179 superfluous feeding, 136-140 Zooplankton, assimilation of nitrogen and phosphorus, 128-140, 164 detritus, 130 dissolved organio material, 130-132 laboratory studies, 132-136 living diets, 129 superfluous feeding, 136-140 Zooplankton, growth in terms of nitrogen and phosphorus, 162172

egg production, 166, 167, 169 net and gross growth efficiencies, 166-172

rate of growth, 162-166, 171 Zooplankton, nitrogen excretion during spring diatom increase, 168 in Clyde sea -a, 166, 167 nutrient regeneration, 160-162 seasonal surveys, 166-160 Zooplankton, phosphorus excretion during spring diatom increase, 158 in Clyde sea area, 166, 167 nutrient regeneration, 160-162 s e a e o d s w e y , 166-160

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Cumulative Index of Authors Allan, J. A., 9, 206 hakawa, K. Y., 8, 307 Balakrishnan Nair, N., 9, 336 Blaxter, J. H. S., 1, 262 Boney, A. D., 3, 106 Bruun, A. F., 1, 137 C m o z , J. E., 6, 1 Cheng, T. C., 5, 1 Clarke, M. R., 4, 93 Corner, E. D. S., 9, 102 Cushing, D. H., 9,266 Cushing, J. E., 2, 86 Davies, A. G., 9, 102 Davis, H. C., 1, 1 Fisher, L. R., 7, 1 Garrett, M. R., 9, 206 Ghirardelli, E., 6, 271 Gullmd, J. A., 6, 1

Hickling, C. F., 8, 119 Holliday, F. G. T., 1, 262 Loosanoff, V. L., 1, 1 Macnae, W., 6, 74 Mauchline, J., 7, 1 Millar, R. H., 9 , 1 Naylor, E., 3, 63 Nelson-Smith, A., 8, 216 Nicol, J. A. C., 1, 171 Riley, C . A., 8, 1 Russell, F. E., 3, 266 Saraawathy, M., 9, 336 Scholes, R. B., 2, 133 Shelbourne, J. E., 2, 1 Shewan, J. M., 2, 133 Sindermann, C. J., 4, 1 Wells, M. J., 3, 1 Yonge, C. M., 1, 209

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Cumulative Index of Titles Artificial propagation of marine fish, 2, 1 Aspects of the biology of seaweeds of economic importance, 3, 106 Behaviour and physiology of herring and other clupeids, 1, 262 Biology of ascidians, 9, 1 Biology of coral reefs, 1, 209 Biology of euphausiids, 7, 1 Biology of wood-boring teredinid molluscs, 9, 336 Blood groups of marine animals, 2, 86 Breeding of the North Atlantic freshwater eels, 1, 137 Diseases of m h n e fishes, 4, 1 Effects of heated effluents upon marine and estuarine organisms, 3, 63 Estuarine fish farming, 8, 119 General account of the fauna and flora of mangrove swamps and forests in the Indo-West Pacific region, 6, 74 Learning by marine invertebrates, 3, 1 Management of fishery resources, 6, 1 Marine molluscs as hosts for symbioses, 5, 1 Marine toxins and venomous and poisonous marine animals, 3, 266 Methods of sampling the benthos, 2, 171 Particulate and organic matter in sea water, 8, 1 Plankton as a factor in the nitrogen and phosphorus cycles in the sea, 9, 102 Present status of some aspects of marine microbiology, 2, 133 Problems of oil pollution of the sea, 8, 216 Rearing of bivalve mollusks, 1, 1 Review of the systematics and ecology of oceanic squids, 4, 93 Scatological studies of the bivalvia (mollusoa),8, 307 Some aspects of the biology of the chmtognaths, 6, 271 Some aspects of photoreception and vision in fishes, 1, 171 Taurine in marine invertebrates, 9, 206 Upwelling and production of fish, 9, 266

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